Вы находитесь на странице: 1из 29

Gumisiriza et al.

Biotechnol Biofuels (2017) 10:11


DOI 10.1186/s13068-016-0689-5 Biotechnology for Biofuels

REVIEW Open Access

Biomass wastetoenergy valorisation


technologies: a review case forbanana
processing inUganda
RobertGumisiriza1*, JosephFunaHawumba1, MackayOkure2 andOliverHensel3

Abstract
Background: Ugandas banana industry is heavily impeded by the lack of cheap, reliable and sustainable energy
mainly needed for processing of banana fruit into pulp and subsequent drying into chips before milling into banana
flour that has several uses in the bakery industry, among others. Uganda has one of the lowest electricity access levels,
estimated at only 23% in rural areas where most of the banana growing is located. In addition, most banana farmers
have limited financial capacity to access modern solar energy technologies that can generate sufficient energy for
industrial processing. Besides energy scarcity and unreliability, banana production, marketing and industrial process-
ing generate large quantities of organic wastes that are disposed of majorly by unregulated dumping in places such
as swamps, thereby forming huge putrefying biomass that emit green house gases (methane and carbon dioxide).
On the other hand, the energy content of banana waste, if harnessed through appropriate waste-to-energy technolo-
gies, would not only solve the energy requirement for processing of banana pulp, but would also offer an additional
benefit of avoiding fossil fuels through the use of renewable energy.
Main body: The potential waste-to-energy technologies that can be used in valorisation of banana waste can be
grouped into three: Thermal (Direct combustion and Incineration), Thermo-chemical (Torrefaction, Plasma treatment,
Gasification and Pyrolysis) and Biochemical (Composting, Ethanol fermentation and Anaerobic Digestion). However,
due to high moisture content of banana waste, direct application of either thermal or thermo-chemical waste-to-
energy technologies is challenging. Although, supercritical water gasification does not require drying of feedstock
beforehand and can be a promising thermo-chemical technology for gasification of wet biomass such as banana
waste, it is an expensive technology that may not be adopted by banana farmers in Uganda. Biochemical conversion
technologies are reported to be more eco-friendly and appropriate for waste biomass with high moisture content
such as banana waste.
Conclusion: Ugandas banana industrialisation is rural based with limited technical knowledge and economic capa-
bility to setup modern solar technologies and thermo-conversions for drying banana fruit pulp. This review explored
the advantages of various waste-to-energy technologies as well as their shortfalls. Anaerobic digestion stands out as
the most feasible and appropriate waste-to-energy technology for solving the energy scarcity and waste burden in
banana industry. Finally, potential options for the enhancement of anaerobic digestion of banana waste were also
elucidated.
Keywords: Banana waste, Waste-to-energy technologies, Biomass valorisation, Bioenergy, Biofuels, Biomass energy,
Anaerobic digestion

*Correspondence: rgumisiriza@cns.mak.ac.ug; rgumisiriza@gmail.com


1
School ofBiosciences, Makerere University, P.O Box7062,
Kampala, Uganda
Full list of author information is available at the end of the article

The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License
(http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium,
provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license,
and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/
publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 2 of 29

Background limited employment opportunities and poverty that are


Globally, energy crisis and proper waste disposal are the major impediments to economic growth [82].
among the major challenges facing most nations [5]. As already pointed out from the foregoing, banana
Uganda is the second largest global producer of bananas production and banana fruit processing are not only
after India and the leading in Africa [164], with annual faced with energy scarcity and unreliability, but also they
production estimated at 9.77 million tonnes [59]. The are accompanied by the generation of vast quantities of
most widely grown cultivars are cooking types belong- waste. Banana Waste (BW) comprises the following frac-
ing to the East African highland banana (EAHB) sub- tions: rotten/damaged fruits, peels, fruit-bunch-stem
group. The other banana cultivars grown in Uganda (stalks), leaves, fibres, pseudo-stem and rhizome [1].
include the dessert bananas locally known as Sukali These fractions of banana wastes are generated from
Ndizi and Bogoya and some other plantain cultivars both, banana production and fruit processing. The waste
for roasting such as Gonja and Kivuuvu while Kay- category generated from the former includes all the off-
inja and Kisubi are mainly for making local beer. The cuts such as pseudo-stem, leaves, fibres and rhizome
EAHB cooking banana (AAA-EA group), locally called that remain in the garden after harvesting fruit bunches,
matooke, is the leading staple food [166] with the annual while the latter generates residues such as peels, fruit-
production of over 6 million tonnes [155]. Banana bunch-stem (stalks) and rotten/damaged fruits. Ugandas
growing in Uganda is either cultivation by smallhold- banana fruit processing alone is estimated to generate
ers in association with other food crops at low densities more than three million tonnes of banana waste annually
(as shade trees for perennials such as coffee) or in com- [155, 166], which means that it is possible to think of the
mercial plantations at high densities in a monoculture waste as a resource for waste-to-energy conversion. Nev-
system. ertheless, banana waste is currently heaped to decom-
Banana processing in Uganda, like other agro-pro- pose in uncontrolled manner thereby emitting large
cessing, relies mainly on costly imported petroleum volumes of Green House Gases (GHGs) especially meth-
products for energy. Cheap and sustainable energy is ane and carbon dioxide that are major drivers of climate
critically essential in banana processing for efficient dry- change. In addition, leachate from BW dump sites con-
ing of banana fruit pulp into chips prior to processing tains high biological oxygen demand and nutrients which
into value-added products such as starch and flour for if channelled into water bodies aggravate climate change
export as well as local food security. Scarlat et al. [145] through eutrophication [83]. Since the main problem of
pointed out that access to cheap, reliable and sustainable banana industrialisation in Uganda is dual comprising:
energy is an important factor that makes agricultural and lack of cheap sustainable energy coupled with the emis-
industrial processes more efficient. For instance, in the sion of large quantities of organic waste residues, yet the
processing of banana, energy would be required for pro- solution to these problems seems to lie in the ability to
cesses such as: drying, milling and also in conversion of convert banana waste into valuable energy. The develop-
the flour into valuable products: starch, bread and cakes, ment of either new or the adaptation of existing waste-
among others. Besides, energy is needed in households to-energy technologies would not only solve the energy
utilities such as cooking, lighting and refrigeration. The needs of the banana industry, but would also eliminate
biggest challenge facing banana industry is the fact that the waste burden with its accompanying environmen-
banana-growing areas, that are concentrated in the rural tal pollution. This review explores the various waste-to-
as well as the remote parts of the country, are not con- energy technologies and evaluates their suitability in the
nected to the national electricity grid. This makes banana generation of energy for use in the banana processing
processing not only expensive but also rather incomplete industry.
as there are many wastages. Typically, electricity distribu-
tion in Uganda is one of the lowest in Africa; estimated Current banana waste utilisation inUganda
at only 912% of the total Ugandan population [99, 162] Banana waste comprises rejected fruits, peels, fruit
and at only 23% in the rural areas [168]. This is compli- bunch stems, leaves, pseudo-stems and fibres. The man-
cated by the fact that most banana farmers have limited agement of banana waste has been largely by cultural
financial capacity to access modern solar energy technol- means such as: (a) direct use pseudo-stems, fibres and
ogies that would generate sufficient energy for industrial leaves to mulch the plantations; (b) banana peels, leaves
processing. Therefore, such limited and unreliable energy and fruit-bunch stalk are composted for manure; and (c)
access translates into underutilisation of the banana banana peels, rejected fruit fingers are fed to animals.
crop, excessive wastage, as well as emission of large vol- However, cultural methods of managing banana wastes
umes of banana waste, leading to the underdevelopment have recently been discouraged due to association with
of the banana industry. This, in turn, contributes to the the rapid spread of plant diseases like the devastating
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 3 of 29

banana bacterial wilt. Applying banana waste from on the flow of hot air over the sliced pulp. Its application
infected banana plants into banana fields as mulches or is, however, hampered by the high energy of operation [6,
compost manure is one of the leading means of trans- 94, 101, 117]. Therefore the conversion of waste biomass
mitting banana bacterial wilt [89, 167]. There have been to energy would offer a cheap and affordable alternative
efforts towards utilising of banana fibres in the produc- source of energy for drying the pulp by banana growers
tion of such products as paper, rope, table mats and and processors.
handbags [137, 112]. Even these efforts are not economi-
cally viable since such products have very short lifes- Waste valorisation: a concept
pan. Hence, utilisation of banana waste through energy Waste valorisation has been defined as the process of
conversions could be the most appropriate venture for converting waste materials into more useful products
Ugandas banana industrialisation. such as chemicals, materials and fuels [13]. Waste val-
orisation as a concept relies on the assumption that even
Energy requirement forbanana processing after the intended use, the residue/waste still contains
Banana processing in Uganda starts with cutting of untapped polymeric substance that can be converted to
mature banana fruit bunches from the pseudo-stems in either energy or other chemical forms. Such products
the plantation. Subsequently, the fruit is de-bunched to make waste a valuable resource that should not be left
separate fruit fingers; the fingers are peeled to get the unharnessed. This concept is currently being applied on
pulp; the pulp is sliced, and finally dried into banana both synthetic waste as well as biowaste, with promising
chips. The banana chips serve as the raw material for success, and it is the basis of the current waste-to-energy
industrial banana processing into value-added products (WtE) approaches. Moreover, due to the fast depletion of
such as starch and flour, for both export and local food natural/primary resources, waste valorisation is not a lux-
security. The drying of banana fruit pulp into chips is ury for academic exploration but rather a much needed
the step that requires reliable energy in order to produce technology for cost-effective and sustainable waste man-
consistently standard quality products. Moreover, it has agement options and generation of renewable energy as
been established [86, 142] that the drying of banana pulp well as production of high-value chemicals such as etha-
consumes more energy than that of other related fresh nol and materials such as nano-bioplastics (Fig.1). Apart
foods such as pineapples and potato. This is so because from renewable energy and high-value chemicals, waste
the activation energy (Ea) for the diffusion of water in valorisation offers additional advantages including: ame-
green banana is 51.21kJ/mol which is higher than that for lioration of waste mal-odours and environmental pollu-
potato (32.24kJ/mol), pineapple (35.17kJ/mol) and grape tion, and reduction of the volume of waste, resulting in
seeds (30.45kJ/mol) [85, 86, 142, 170]. The differences in
the activation energy values can be attributed to the dif-
ferences in the chemical composition and cellular struc-
ture [86]. In Uganda, the drying of banana pulp is done
by directly spreading fresh banana fruit pulp on the mat
and exposed directly to sunshine. Nevertheless, although
Uganda is located on the equator, the number of hours
of sunshine per day varies significantly depending on the
season. During rainy season, there are few hours of sun-
shine that make the traditional drying method take many
days resulting in the pulp either rotting, or infested with
moulds that produce aflatoxins. Aflatoxin contamination
is one of the major hindrances to the development of the
banana industry as the products thereof would not meet
the minimum standards for human consumption. There-
fore direct sunshine drying, as done locally, does not
meet the energy requirements for efficient and safe dry-
ing of the pulp for subsequent processing. Other options
would be: (a) the use of modern solar dryers. This, how-
ever, has not been massively adopted due to the high cost
of installation and (b) hot air convection drying. This is
one of the oldest methods that have been used to pre- Fig.1 A scheme of green processing technologies for waste valorisa-
serve agricultural products like banana [143] and relies tion [13]
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 4 of 29

the recovery of more space for other uses. In a typical As already mentioned in the foregoing, the WtE options
process, high-value chemicals are produced from waste are most preferred due to recovery of energy that can
residues through any of the four downstream processing offset the cost of waste treatment. The energy content
i.e. using inorganic and organic chemicals, a combination of waste is usually recovered by means of either thermo-
of chemicals and enzymes, biotechnological approach chemical processes such as combustion, pyrolysis and
using genetically engineered organisms, and green pro- gasification or biological processes such as anaerobic
cessing technologies whereby only water is used as a rea- digestion. A possible algorithm (Fig. 2) for selecting or
gent in waste volarisation [13]. developing a suitable WtE technology has been described
Waste-to-Energy (WtE), defined as the process of recov- by Stehlik [156]. In this algorithm, the waste is first
ering energy in the form of either electricity and/or heat assessed for its suitability for thermal processing due to
from waste, [30] applies the waste valorisation concept ease of application of thermal conversion technologies.
to generate renewable energy such as heat and biofuels Wastes that cannot be appropriately degraded by thermal
(biogas, syngas and bioethanol). Waste-to-Energy tech- means, the emitting industry either employs the existing
nologies are categorised into two major groups namely; non-thermal convenient technologies such as anaerobic
(a) thermo-chemical processes comprising combustion, digestion or supports research for development of new
pyrolysis and gasification; and (b) biological processes com- WtE technologies tailored to the type of waste emitted.
prising anaerobic digestion and bioethanol fermentation. On the other hand, wastes that are suited for degradation
These WtE technologies provide cheap sources of energy by thermal means are further evaluated for use as alterna-
that is crucial for industrial processes such as drying, pack- tive fuels. Wastes that are not amenable for use as alter-
aging and preservation industrial products. As already native fuel are degraded via incineration while for those
highlighted, the banana industry releases a large volume of that conform to use as alternative fuel are converted to
waste that is currently neglected and left to decompose in energy via other WtE technologies such as pyrolysis,
an uncontrolled manner. Besides, the development of this gasification as well as thermo-mechanical pulverisation
industry is hampered by both scarcity and costly energy to form refuse-derived fuel. Furthermore, the algorithm
inputs. The application of this volarisation concept, par- supports the need for research and development of new
ticularly the green processing options, would solve both technologies in order to either improve on the efficiency
of these hindrances to the banana industrial development. of the available technologies and/or innovate new appro-
Scarlat etal. [145] reported that the energy content of such priate WtE technologies for waste management. These
wastes as banana waste can be recovered by employing new technologies need to prove their economic viability
appropriate WtE technologies. A number of studies have prior to full-scale implementation. Generally, the simpler
been conducted to establish the best way to harness energy design has low propensity for technological failure.
from banana waste. For instance, banana wastes have
been used to make briquettes that store energy for further Potential WtE technologies forbanana waste
uses in industrial and domestic heating [98, 149, 183]. In valorisation
a separate study, Tock et al. [163] applied direct combus- The potential WtE technologies that can be used in the
tion of pseudo-stems and leaves to generate heat energy. valorisation of BW can be grouped into: Thermal (Direct
The green processing option has been attempted [44, 163] combustion and Incineration), Thermo-chemical (Tor-
whereby microorganisms have been employed to anaerobi- refaction, Plasma treatment, Gasification and Pyrolysis)
cally convert banana peels into methane, in one study, and and Biochemical (Composting, Ethanol fermentation and
banana fruit residues fermented into ethanol [64, 74, 179] Anaerobic Digestion) [30] Fig.3. Generally, thermal tech-
in another study. Thus, recovery of energy from waste can nologies convert the waste directly into heat energy while
play a role in minimising the impact of waste on the envi- thermo-chemical and biochemical ones first convert the
ronment with the additional benefit of providing a local waste into secondary energy carriers such as syngas, tor-
source of cheap energy [145]. refied pellets, biogas, bioethanol and biooil, which can
Development of innovative technologies with high WtE subsequently be burnt (in furnaces, steam turbine, gas
efficiencies is largely dependent on two major but inter- turbine or gas engine) to produce energy in the form of
linked factors namely, the type of waste to be harnessed heat and/or electricity. The conversion of solid wastes
[174] and the available legislation. The legislation for into secondary energy carriers allows for a cleaner and
environmental pollution abatement compels the waste more efficient energy harnessing process.
sources (industries) to employ the most eco-friendly
technologies for waste management. In addition, the Thermal conversion technologies
physico-chemical nature of the waste dictates the choice This is the full oxidative combustion of waste biomass
of the technology appropriate for treating such a waste. mainly to generate heat energy. This is done by either
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 5 of 29

Fig.2 Algorithm for convenient WtE technology selection [156]

direct combustion or incineration. Direct combustion called an incinerator with the purpose of generating
is the burning of biomass directly to convert chemi- thermal energy and simultaneous destruction of patho-
cal energy stored in plants into heat and electricity genic waste material under emission control. During
[45]. The direct burning of dry biomass to generate incineration, the biomass is converted either directly
heat energy for mainly cooking and lighting has been into CO2 and water vapour or indirectly into CO, H2
practised globally for years. Dry banana waste such as and Char (Fig. 4). The concentration of oxygen avail-
leaves, fibres and fruit-bunch-stems can be used as a able for the process is the major determining factor.
source of heat energy in domestic cooking and indus- The direct step is favoured at higher oxygen concentra-
trial boilers. Industrially, biomass is burnt in the fur- tions while the latter occurs when there is limited oxy-
nace to generate thermal energy that subsequently gen supply. Waste incineration is common practice in
heats boiler to produce steam. The pressure of the the developed countries (EU, US, Japan) where waste-
steam can be used to turn a turbine that is attached related policies limit waste disposal on land [145].
to an electrical generator which subsequently gener- Although waste incineration appears simple and appli-
ates electricity [37]. The potential of banana residue cable for Ugandas banana processing waste, the tech-
to be directly combusted for energy generation strictly nology can be challenged by a number of bottlenecks.
depends on its energy content or heating value [163]. The high capital, maintenance and operation costs of
However, banana residues have very high moisture waste incineration plants prevent the large-scale appli-
content which lead to low net energy efficiency when cation of this technology as an energy recovery option
combusted without prior drying process. Moreover, [171, 172]. As with direct combustion, incineration is
open burning of waste is particularly discouraged due also affected by the high moisture content of banana
to the emission of harmful compounds such as diox- waste, which makes continuous and optimal plant oper-
ins, acid gases and furans that cause air pollution [145]. ation difficult to achieve owing to the requirement of
Hence, direct combustion is not a suitable technology additional fuel to support the process. Besides, without
for harnessing energy from banana biomass. proper controls, waste incineration can be highly pol-
Waste incineration, on the other hand, is a full oxida- luting, generating harmful emissions, such as dioxins
tive combustion of the waste in an engineered structure and heavy metals.
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 6 of 29

Fig.3 Potential WtE technologies for valorisation of banana waste [30]

require strict control of process conditions in specially


designed reactors that are able to separate tempera-
ture accordingly. Without temperature separation and
proper air rationing, thermo-chemical reactions do not
occur ultimately, turning the process into incineration or
combustion.
Fig.4 Key reaction steps and products from biomass combustion Pyrolysis and gasification differ from incineration in
that the former may be used for recovering the chemi-
cal value of the waste, while the latter is used to recover
its energy value. The chemical products generated from
Thermochemical conversion technologies pyrolysis and gasification may be either used as fuel to
Unlike incineration and open combustion, thermo- generate heat energy or as secondary feedstocks (char)
chemical conversion technologies employ a series of for subsequent fuel generation (Fig. 6). The products
chemical reactions occurring at different temperatures from incineration are generally non-fuel and include ash
and may require partial oxidation as in gasification or and flue gas that mainly consists of carbon dioxide and
proceed in the absence of oxygen as in pyrolysis. These water vapour.
conversion technologies are temperature depended Like incineration, pyrolysis and gasification also release
and proceed through overlapping spatial and temporal carbon dioxide. A comparison of pyrolysis, gasification
stages of drying and degassing, pyrolysis and gasifica- and combustion based on generated products is shown
tion and finally full oxidative combustion that turns the in Table 1. The principles underlying the application of
organic waste into ash (Fig. 5). All these technologies each of the thermo-chemical conversion technologies
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 7 of 29

Fig.5 The temperature overlapping of thermo-chemical conversion technologies

Fig.6 Sequential product generation during pyrolysis and gasification

Table
1Thermo-conversion processes and products in harnessing energy from biomass are here below
(Adapted from Bridgwater [32]) described in detail:

Pyrolysis
Pyrolysis is the thermal degradation of organic mate-
rial in the absence of oxygen. It occurs at relatively low
temperatures (400900 C) [30]. In pyrolysis, biomass
is subjected to an optimal temperature of 700 C in
the absence of oxygen resulting in the production of
pyrolysis oil (biooil), char and synthesis gas (Syngas).
Syngas is a mixture of majorly CO, CO2, H2, H2O, CH4,
trace amounts of higher hydrocarbons such as ethane
and propane, as well as various contaminants such as
small char particles. These can be used as secondary
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 8 of 29

fuel to generate electricity. In a typical process the Gasification


biomass is transformed into high quality fuel without Gasification is a partial oxidation of organic substances
creating ash or emitting large volumes of flue gas as at elevated temperature (5001800 C) to produce syn-
in combustion. The process proceeds through the fol- gas. Biomass gasification occurs as the char reacts with
lowing basic process stages: (1) grinding to increase carbon dioxide and water vapour (steam) to produce car-
the surface area for improved heat transfer and reac- bon monoxide and hydrogen via the reaction Eqs. 36
tion; (2) drying to increase the efficiency of gassolid (Fig. 7). In addition, the concentrations of carbon mon-
reactions within the reactor; (3) anoxic thermal deg- oxide, steam, carbon dioxide and hydrogen are balanced
radation of organics to generate pyrolysis products very fast at the temperatures in a gasifier via the equilib-
(pyrolysis gas, biooil and char); and (4) ultimate sec- rium reaction Eq.7 (Fig.7). Syngas can be used as a fuel
ondary treatment of pyrolysis gas and pyrolysis char. for efficient production of electricity and/or heat [169]. A
The last step involves the condensation of the gases for gasifier can use oxygen, steam, carbon dioxide or a mix-
the extraction of energetically usable oil mixtures and/ ture of these as gasification agents.
or combustion of gas and char as secondary energy On the other hand, banana waste being a wet biomass
products. The major gases generated from pyroly- is not regarded as a promising feedstock for direct utilisa-
sis are methane, carbon monoxide and hydrogen and tion or application of the conventional thermo-chemical
are shown by reaction Eqs. 1 and 2 (Fig. 7). Pyrolysis gasification processes due to its high moisture content
offers a flexible and attractive way of converting solid [163]. This problem can be circumvented by employing
biomass into an easily stored and transportable fuel, a recently developed technology referred to as supercriti-
which can be successfully used for the production of cal water gasification (SCWG) whereby water is used as a
heat, power and chemicals. Pyrolysis gas, for example, reaction medium. In this technology, gasification of wet
may be used to power gas engines and gas turbines to biomass may be accomplished without having to dry the
generate electricity more efficiently than conventional material and thereby avoiding the high processing costs
steam boilers. Moreover, pyrolysis of biomass may lead associated with the drying process. Supercritical water
to the recovery of organic liquid fraction as fuel in the gasification of wet biomass, as an advanced technology,
form of methanol that can be distilled for use in vari- has drawn the attention of a few research groups in the
ous industries. Notably too, combustion of pyrolysis USA, Germany, Japan and the Netherlands [163]. The
products emits smaller volumes of flue gas compared main advantage of using SCWG is that the technology
to direct combustion and incineration of biomass does not require drying of wet biomass prior to gasi-
and hence pyrolysis reduces the flue gas treatment fication [62]. As a matter of fact, water in wet biomass
capital costs. Despite the advantages of pyrolysis, bio- is essential for the chemical reactions. Moreover, the
mass with high ash content such as straw and banana SCWG of wet biomass results into high yields of hydro-
waste are not good feedstocks for pyrolysis process gen (H2) and very low yield of carbon monoxide (CO)
due to reactor blockage by ash accumulation. Besides, when compared to the dry processes in which syn-
pyrolysis is an expensive technology that requires high gas is produced with CO as the main product. Besides,
investment costs before it can be carried out commer- in SCWG less tar and coke are formed and inorganic
cially for energy harnessing. ingredients such as salts remain in aqueous solution,
thus corrosion problem during gas treatment can be
avoided. Nevertheless, SCWG is an expensive technology
which requires high capital investment before put into
operation.

Plasma technology
Plasma technology relies on the physical principle that
matter changes its state when energy is supplied to it:
solids become liquid, and liquids become gaseous. When
more energy is supplied to a gas, it is ionised and goes
into the energy-rich plasma state, the fourth state of mat-
ter [126]. The initial energy required to create plasma
can either be thermal or electric current or electromag-
netic radiations. The presence of charged gaseous spe-
Fig.7 Major reactions of pyrolysis and gasification conversion cies makes the plasma highly reactive and causes it to
technologies behave significantly different from other gases, solids
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 9 of 29

and liquids. The peculiar advantage of this technology concentrated into an energy-dense and homogeneous
is that the energy contained in the plasma allows the product (TOPs) useful for further thermo-chemical con-
use of low energy biomass that would otherwise not be versions [188]. Torrefaction technology is also referred to
suitable as feedstock for energy generation using gasi- as mild pyrolysis and is a thermo-chemical process con-
fication technology. The high-temperature conditions ducted in the temperature range between 200 and 300C
that are reached in plasma results in the decomposition under an inert atmosphere and low heating rate [110].
of organic compounds into their elemental constituents The process involves biomass chipping to allow efficient
and ultimately forming a high-energy synthesis gas, con- drying, screening for impurities before sizing [148] and
stituted mainly of hydrogen and carbon monoxide. Nev- drying to 20% moisture content (Fig.8). A small fraction
ertheless, the application of plasma-based systems for of the feedstock biomass is used as fuel for the drying
waste management is challenging. For instance, the use of and torrefaction process. Torrefied biomass (briquettes)
electricity as an initial energy vector is expensive, turning which retains upto 96% of its chemical energy is hydro-
economic considerations into the strongest barrier for phobic and resistant to biodegradation. Therefore it can
using plasmas for waste treatment. Moreover, the inor- be used as substitute for coal/charcoal for domestic heat-
ganic fraction (glass, metals and silicates) that is melted ing, co-firing power generation and gasification [3, 135,
and converted into a dense, inert, non-leaching vitrified 139]. A study by Sellin etal. [149], in the Northern region
slug can be hazardous when released to the environment. of Santa Catarina in Brazil, revealed that banana wastes
including leaves and pseudo-stems can be used to pro-
Torrefaction duce briquettes as fuel for energy generation. Briquettes
Torrefaction is defined as the thermal upgrading of bio- produced from this waste at low cost are an excellent
mass into a more homogeneous product that is densified source of cheap renewable energy which is regarded as
through pelletisation to generate a more energy-dense environmentally clean. Despite the potential of torre-
product called torrefied pellets (TOPs) or briquettes, faction technology, there are still several technical and
with similar properties to coal [19]. The energy derived economic challenges that need to be overcome before
from biomass through thermal upgrading (heating) is the technology is fully commercialised in the banana

Fig.8 A flow scheme of an integrated torrefaction process based on [19]


Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 10 of 29

industry [127]. Firstly, banana waste like other plant bio- Biochemical conversion primarily involves the action of
mass is highly heterogeneous in quality and nature, and enzymes derived from microorganisms to harness the
is mostly available in low energy density form [50, 123, energy stored in biomass. The techniques falling under
181]. Secondly, it has relatively high moisture content this category are: composting to generate heat energy,
and consequently lower heating value compared to fossil bioethanol fermentation and anaerobic digestion for
fuels [24, 40, 136]. It, therefore, needs to be pre-treated biogas production.
to improve handling [104, 131, 140]. Pre-treatment such
as pre-drying to 20% moisture content is energy consum- Composting
ing and significantly reduce the energy efficiency of the Composting, defined as the biological decomposition of
technology. biodegradable solid waste under predominantly aerobic
conditions, transforms the biomass into: carbon dioxide,
Biochemical conversion technologies water, heat and a more stable solid product called com-
Biochemical conversion technologies of waste-to-energy post. The compost is nuisance-free, easy to handle and
are much more eco-friendly as compared to the thermal can be safely used in agriculture to ameliorate the soil
and thermo-chemical techniques discussed in the fore- [12, 84, 90]. Recently, there has been increased atten-
going. The advantages and disadvantages of different tion given to heat recovery from aerobic composting sys-
waste-to-energy technologies are highlighted in Table2. tems as a way to improve their economic viability [154].

Table2 Advantages anddisadvantages ofdifferent WtE technologies [90]


Technology Advantages Disadvantages

Anaerobic digestion Energy recovery with the production of high grade soil Unsuitable for wastes containing less organic matter
conditioner
No power requirement for sieving and turning of waste pile Requires waste segregation for improving digestion effi-
ciency
Enclosed system enables trapping the gas produced for use
Controls GHG emissions
Free from bad odour, rodent and fly menace, visible pollu-
tion and social resistance
Compact design needs less land area
Net positive environmental gains
Can be done in small scale
Landfill with gas recovery Least cost option Surface runoff during rainfall causes pollution
Gas produced can be utilised for power generation or direct Soil and groundwater may get polluted by the leachate
thermal application
Skilled personnel not required Yields only 3040% of the total gas generated
Natural resources are returned to the soil and recycled Large land area required
Can convert marshy lands to useful areas Significant transportation costs
Cost of pre-treatment to upgrade the gas to pipeline quality
and leachate treatment may be significant
Spontaneous explosion due to methane gas buildup
Incineration Most suitable for high calorific value waste Least suited for aqueous, high moisture content, low calorific
value and chlorinated waste
Units with high throughput and continuous feed can be Toxic metal concentration in ash, particulate emissions, SOx,
set up NOx, chlorinated compounds, ranging from HCL to dioxins
Thermal energy for power generation or direct heating High capital and O&M costs
Relatively noiseless and odourless Skilled personnel required
Low lands are required
Can be located within city limits, reducing transportation
costs
Hygienic
Pyrolysis/Gasification Production of fuel gas/oil, which can be used for various Net energy recovery may suffer in waste with excessive
purpose moisture
Control of pollution superior as compared to incineration High viscosity of pyrolysis oil may be problematic for its burn-
ing and transportation
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 11 of 29

Generally, the composting process is optimised by having system that ultimately dictates the temperature within
the starting carbon to nitrogen ratio in the range of 30:1 the composting substrate. A study by Smith and Aber
and the moisture and oxygen levels and temperatures [154] reported an operational system capturing thermal
that are closely managed and monitored [58]. Three cat- energy in the hot air generated by the composting pro-
egories of microorganisms, namely, bacteria, actinomy- cess, installed at the research farm of University of New
cetes and fungi are involved in the composting process. Hampshire (UNH) in the United States.
In the initial phase of composting, mesophilic microor- The system consists of an aerated static pile (ASP) of
ganisms such as bacteria, Bacillus, Clostridium, Alcali- biomass or compost housed in a concrete insulated com-
genes, Serratia and Pseudomonas, degrade biomass. This post bay (Fig. 10). The hot vapour from the ASP is col-
is accompanied by the generation of heat owing to their lected through PVC pipes that passes through manifold
metabolic activities, causing the ensuing rise in tempera- and connects to the heat exchange system. The conden-
ture (45C) in the composting heap. This gives way to sate from the manifold and heat exchange system is col-
the second phase, whereby thermophiles take over the lected through condensate sump and ultimately pumped
composting process. Thermophilic fungi such as Asper- back to the ASP in the compost bay. The heat exchange
gillus fumigates, Humicola sp, sporotrichum thermophile system operates by blowing hot compost vapour (110
and Myriococcum thermophilum, and Streptomycetes 170 F), against an array of two-phase super-thermal
thermofuscus, S. Rectus, Nocardia sp and Thermoactino- conductor heat pipes termed as Isobars. These Isobars
myces sp continue with the process until the temperature are 30 ft long containing within 24-in. diameter vapour
of50C is reached above which most of them are either duct and housed inside a 295-gallon water tank. Isobars
inhibited or remain dormant as spores. Above 50C the- provide thermal uniformity across the entire length of
mophilic bacteria belonging to such genera as Bacillus the pipe, thus heat energy is evenly distributed across
(Bacillus stearothermophilus), Thermus, Clostridium con- the entire length of the pipe [2]. When compost heated
tinue with the process to temperatures ranging from 60 vapour is applied to the evaporator side of the pipe (por-
to as high as 65C (Fig.9) and then starts to fall within tion contained within the 24-in. diameter pipe), the
a couple of months [152]. This sets in the third and final refrigerant inside the Isobar heats up and vapourises. The
phase of the composting process. During this final stage, vapour stream within the Isobar travels up the pipe, con-
the actinomycetes, initially, followed later by fungi pro- densing on the cooler side, releasing its energy in the bulk
ceed with the composting process until the temperature storage water tank through the latent heat of condensa-
falls to mesophilic range, after which both mesophilic tion. After condensing, the refrigerant is returned to the
fungi and bacteria re-colonise the compost heap to com- warm end of the pipe through gravity, repeating the pro-
plete the process. cess without any moving parts.
The mechanism of heat transfer has been described The system captures the metabolic heat produced by
by Shaw and Stentiford [151]; Themeli [161] and Tucker microorganisms during aerobic composting, through a
[165] and involves convection and conduction, with radi- negatively aerated fan system, and blows the hot compost
ation effects being assumed negligible. There are three vapour (110170F) against the heat exchange system to
components of energy balance namely; energy trans- heat water for radiant floor heating, feed preparation and
fers into, within and out of a composting system which sanitation of equipment. However, the success in appli-
together equate to the change in energy stored within the cation of composting technology to generate thermal
energy has been scantily reported elsewhere in the world.
Moreover, composting of mixed wastes generates low
quality compost which can introduce heavy metals into
human food chain.

Bioethanol fermentation
Ethanol produced from different renewable feedstock
constitutes an alternative fuel for spark ignition engines
[179]. This ethanol is considered as biofuel due to the
vegetative origin of its carbon and, therefore, when it is
released during the combustion process, it will not con-
tribute to the increase in CO2 emissions [76, 88]. The
most suitable feedstock for ethanol production are high
sugar-content crops such as sugarcane, sugar beets and
Fig.9 Heat generation during composting fruits, since they majorly contain simple sugars such as
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 12 of 29

Fig.10 Flow diagram of UNH heat recovery system [154]

glucose and fructose, that can be readily converted into starch-based crops such as corn, grains and potatoes,
ethanol by alcohol-fermenting microorganisms [56]. Two among others, involves the enzymatic breakdown of
groups of microbes: saccharolytic and ethanologenic, are strong 1,6 glycosidic bonds in starch into simple sugars
important in ethanol production. These groups oper- (glucose) prior fermentation into ethanol [150]. On the
ate on the principle of co-metabolism, whereby, when other hand, lignocellulosic feedstock such as banana
saccharolytic microbes break down complex polymeric fruit-bunch-stem contains cellulose, hemicellulose
carbohydrates (starch, cellulose, hemicelluloses, etc.) and lignin which are more difficult to breakdown than
to simpler utilisable forms the ethanologenic converts starch and may require concerted efforts involving con-
them to ethanol. Many promising saccharolytic and etha- sortia of microorganism. While one consortium may
nologenic microbes fall within, respectively, the phyla breakdown the lignin wall, another may be required to
Neocallimastigomycota and Ascomycota, for fungi, Pro- hydrolyse the polymer into simpler units for the next
teobacteria and Fibrobacteres, for bacteria. Notably, Sac- consortium. Details of the interplay of these microbial
charomyces cerevisiae. (Ascomycota) and Zymomonas consortia are covered below under the pre-treatment
mobilis (Proteobacteria) are the only microbes naturally options. Nevertheless, the application of bioethanol
capable of producing ethanol close to theoretical maxi- fermentation as a waste-to-energy approach has limita-
mum, with Saccharomyces cerevisiae predominant for tions. For instance, conversion of biomass into bioetha-
current ethanol production based on starch and sugar nol generates other forms of highly polluting wastes
feedstocks. such as distillery slope that cannot be directly applied
To enable cellulosic ethanol technologies, microbial to the fields as biofertiliser or bioslurry. Moreover, the
capability and efficiency must be enhanced by appro- use of bioethanol as engine fuel for generating electric-
priately designed mixedculture systems and/or geneti- ity negatively affects the electric fuel pumps by increas-
cally modified microbes. Since banana-associated ing internal wear and undesirable spark generation. In
residual biomass are generally starchy (amylaceous) addition, ethanol is hygroscopic a property that makes
and lignocellulosic materials; they can give high yields it absorb water from air leading to high corrosion
of glucose after successful hydrolysis which may further progression of energy generating engines and power
be fermented to produce ethanol. The conversion of machines [107].
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 13 of 29

Anaerobic digestion as sugars, amino acids, fatty acids and glycerol. It should
Biochemical and microbial fundamentals of anaerobic be noted that organic wastes are a complex mixture of
digestion (AD) Anaerobic digestion (AD) is the anoxic mainly carbohydrates (starch cellulose, hemicellulose),
biological decomposition of organic matter by a complex proteins and lipids; with their relative concentrations
microbial ecosystem through parallel sequences of meta- being dependent on the nature and origin of the waste.
bolic pathways involving different kinds of synergistic Owing to their structural complexity, the biopolymers
microbial trophic groups leading to the formation of meth- are not only too large for microbial uptake through the
ane and carbon dioxide [66]. The mixture of methane and cell membrane for the subsequent intracellular biotrans-
carbon dioxide is referred to as biogas [42, 43]. Anaero- formation steps, they are also either sparingly soluble or
bic digestion offers the opportunity to produce renewable completely insoluble in aqueous medium. Therefore, in
energy and a higher quality of treatment for agro-waste. order to utilise these biopolymeric organics, uptake must
The technology has recently become an attractive method hydrolyse them to smaller units and solubilised, to enable
in Europe for the biodegradation of organic fractions membrane uptake and their availability to further meta-
derived from municipal solid waste [145]. The AD process bolic degradation.
is driven by concerted action of highly varied microbial Biopolymer hydrolysis is accomplished by means of
population, consisting of several groups of both strict and extracellular hydrolytic enzymes such as laccase, cel-
facultative bacterial strains. The process is carried out in lulases, amylases, proteases and lipases, which may be
well-designed vessel referred to as anaerobic digester/ either secreted into the environment or secreted but
anaerobic bioreactor. The entire system consisting of the remain bound to cell membrane as protuberances [108,
feedstock, digester, biogas holder and digestate reservoir 114, 115, 130]. In the digester system, both mesophilic
is called a biogas plant. The complete AD process of a and thermophilic microbes work synergistically to hydro-
lignocellulose-rich substrate such as banana waste can be lyse the biopolymers into simple units (oligomers and
divided into four main stages (Fig.11) namely: hydrolysis, monomers). For instance, after the pre-treatment step,
acidogenesis (or fermentation), acetogenesis and metha- the lignin layer would have been removed thereby expos-
nogenesis. ing cellulose, which is a substrate to a number of bacterial
genera in the digester. Clostridium Acetivibrio, Bacte-
(a) Stage one: Hydrolysis roides, Selenomonas and Ruminococcus are some of the
most common hydrolytic bacteria in the anaerobic bio-
During hydrolysis, the insoluble complex biopolymers reactors [16, 17]. In the rumen, the most similar natural
such as polysaccharides, proteins and lipids are broken environment to biodigesters, Ruminococcus albus and
down into simple soluble monomeric biomolecules such R. flavefaciens are the predominant gram-positive, fibre-
degrading bacteria, while Fibrobacter succinogenes is the
most abundant gram-negative [180]. Typically, hydro-
lytic bacteria adhere to the substrate particles, which
subsequently induce the production and secretion of the
specific hydrolytic enzymes. Starch is broken down by a
mixture of amylolytic enzymes that hydrolyse the -1,4
and -1,6 glucosidic bonds of amylose and amylopectin.
This enzyme mixture includes - and -amylase, which
exhibit specificity to -1,4 glycosidic bonds, and glu-
coamylase (amyloglucosidase), which exhibit specificity
to both the -1,4 and -1,6 glucosidic bonds [29, 100].
Starch hydrolysis releases a mixture of sugars; notably
maltose and glucose. On the other hand, cellulases which
are sub-divided into three main groups namely: endocel-
lulase or endo--1,4-d-glucanase, (EC 3.2.1.4), exocel-
lulase or exo--glucanase, also called cellobiohydrolase
(EC 3.2.1.91) and -glucosidases (EC3.2.7.21), are also
secreted by microorganisms in the digester. The degra-
dation of cellulose is effected by the cooperative action
of both endocellulase and exocellulases, whereby, the
Fig.11 Scheme of anaerobic biodegradation process of lignocel- endocellulases randomly hydrolyse internal glycosidic
lulosic substrate linkages, which are accompanied by a rapid decrease
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 14 of 29

in polymer length and gradual increase in the reducing typical of the rumen include species of Clostridium and
sugar concentration, while the exocellulases hydrolyse R. Albus [49, 153], while Streptococcus sp., Lactobacillus
the oligosaccharides released by the endocellulases to sp. and Propionibacterium are also fermentative microor-
produce cellobiose from a non-reducing end. Completed ganisms associated with the biodigesters, probably origi-
hydrolysis is achieved when -glucosidase hydrolyses nating from the environment. Their degradative products
cellobiose to glucose monomers [75, 102]. The cellulase of metabolism include acetate, lactate, ethanol, CO2 and
enzyme system is enclosed in a cellulose-binding mul- H2 [81]. On the other hand, the deamination process in
ticellulase-containing protein complex called a cellulo- the degradation of amino acids also produces ammo-
some. The cellulosome is responsible for the adherence nia. Microbial fermentation of glucose and 5-carbon
of the bacterial cell to cellulose and to hydrolyse the cel- atom sugars such as xylose and ribose mainly proceed
lulose thereafter. It should also be noted that the cellulo- through EmbdenMeyerhof Pathways (EMP), generating
some complex retains the ability to bind to and hydrolyse pyruvate as an intermediate pathway product. However,
cellulose when present in the extracellular medium as it the formation of pyruvate depends on the conditions
does when it is cell bound [22, 23]. Similar surface struc- prevailing in the bioreactors and the microbial species
tures exist among different cellulolytic bacteria. Typi- present. Pyruvate is a central molecule in terms of bio-
cal examples include: (a) glycocalyses, which have been chemical interconversions and can be converted into dif-
observed in rumen bacteria, (b) fibrous and membranous ferent compounds such as acetate, propionate, butyrate,
structures of Bacteroides succinogenes and (c) spherical formate, lactate, alcohols, ketones and aldehydes [133].
bodies, vesicular structures, lobes and tubelike append- The amino acids originating from protein hydrolysis
ages, which have been observed in Ruminococcus albus. can be degraded either through fermentation follow-
The presence of these structures strongly supports the ing either stickland reactions or via anaerobic oxidation
widely held view that a single enzyme is incapable of linked to hydrogen production. The protein biodegrada-
extensive solubilisation of complex substrates, but rather, tion products are volatile fatty acids (VFAs), ammonia,
multiple enzyme system that act synergistically are sulphide, carbon dioxide and hydrogen depending on the
required (113). Microorganisms produce both intracel- amino acid present, microbial diversity and the pathway.
lular and extracellular proteases contemporaneously [71]. Butyrate and valerate are typical products of valine and
As with other classes of enzymes, proteases likewise, play leucine amino acid biodegradation [33, 109, 125]. The
major roles in microbial physiology and as such, their acidogenic microbial population can constitute upto 90%
production is highly regulated to suit particular needs. of the total microbial populations present in the anaero-
The synthesis of extracellular proteases, for example, is bic digesters [134]. These microbes have a short doubling
also tightly regulated. Their production has been linked time that makes acidogenesis not regarded as a limiting
to their participation in physiological activities such as step in the process of anaerobic digestion.
sporulation [138], cell wall turnover and autolysis [157],
nutrition and overall protein turnover [105]. Lipases (tri- (c) Stage three: Acetogenesis
acylglycerol acylhydrolase; EC.3.1.1.3) hydrolyse lipids
or triacylglycerols to diacylglycerides, monoacylglycer- Acetogenesis is the degradation of reduced fermenta-
ols, fatty acids and glycerol. In comparison, hydrolysis of tion intermediates (electron sink) from the previous
proteins and lipids is faster [128]. Proteins are generally stage, i.e. volatile fatty acids (VFAs) such as propionate
hydrolysed to amino acids by proteases. Microorganisms and butyrate to acetate, carbon dioxide and hydrogen by
that are responsible of this reaction include species of the obligate hydrogen-producing acetogens (OHPA). This
genera Bacteroides, Butyrivibrio, Clostridium, Fusobacte- intermediate bioconversion is a crucial process for the
rium, Selenomonas and Streptococcus [8]. successful production of biogas, since these compounds
cannot be utilised directly by methanogens. However, the
(b) Stage two: Acidogenesis acetogenic reactions (Table 3) are not energetically fea-
sible under standard conditions because the reactions
In acidogenesis, soluble monomers: simple sugars, are energy consuming (endothermic; +ve values of G).
amino acids, glycerol and fatty acids released from the Therefore, a syntrophic microbial interdependency is
hydrolysis stage, are biodegraded by fermentative organ- required for the reactions to proceed.
isms and anaerobic oxidisers (-oxidisers) to produce According to Bjrnsson [27] and Cirne [42], the reac-
different organic acids. Representatives of domain Bac- tions become feasible when the hydrogen partial pressure
teria, especially microbial genera inhabiting the rumen: (PH2) is low (104105 atm). Acetogens are slow-grow-
Clostridium, Eubacterium and Bacteroides, are largely ing microorganisms and depend on a low hydrogen par-
responsible for acid generation. Fermentative species tial pressure in order for acetogenic biodegradation to
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 15 of 29

Table3 Free energy values of key acetogenic and methanogenic reactions of anaerobic digestion (Adapted from [42,
108])
AD step Reaction G0 (kJmol1)*

Acetogenesis
PropionateAcetate CH3 CH2 COO + 3H2 O CH3 COO + H+ + HCO
3 + 3H2 +76.1
ButyrateAcetate CH3CH2CH2COO+2H2O2CH3COO+H++2H2 +48.1
EthanolAcetate CH3CH2OH+H2OCH3COO+H++2H2 +9.6
LactateAcetate CH3CHOHCOO + 2H2 O CH3 COO + H+ + HCO
3 + 2H2 4.2
FormateAcetate 2HCO +
3 + 4H2 O + H CH3 COO + 4H2 O 104.6
Methanogenesis
AcetateMethane CH3 COO + H2 O HCO
3 + CH4 31.0
H2/CO2Methane 4H2+CO2CH4+2H2O 131.0
FormateMethane HCO +
3 + 4H2 + H CH4 + 3H2 O 135.6
*Temperature 298K, pH 7, 1M for solutes and 1atm for gases

yield energy required to move the reaction forward [27]. phenigii [42]; (c) the primary alcohol-degrading bacteria
This low (PH2) is achieved by the syntrophic associa- encompassing such species as: Syntrophobacter fumar-
tion of obligate hydrogen-producing acetogens (OHPAs) oxidans, Desulfovibrio vulgaris, Thermoanaerobacterium
with hydrogen-consuming bacteria (hydrogen scaven- brockii and Pelobacter venetianus; and (d) homoace-
gers) such as the hydrogenotrophic methanogens [147]. togenic bacteria (hydrogen utilising acetogens such as
However, the thermodynamic feasibility of acetogenic strain AOR) which are responsible for converting acetic
reactions is inversely proportional to that of methano- acid into hydrogen and carbon dioxide. Acetogenesis is a
genic reactions. This means that hydrogen-producing low energy-yielding anaerobic biodegradation step. This
acetogenic reactions become more favourable at low PH2 makes acetogenic microbes very slow growing and sen-
(Fig. 12) whereas hydrogen-consuming methanogenic sitive to changes in organic loads, flow rate and environ-
reactions become less favourable at the same PH2. Thus, mental conditions [186]. Acetogenic bacteria, therefore,
syntrophic reactions occur within a narrow range of very require long periods to adapt to new environmental con-
low PH2 (between 104 and 105 atm). ditions in order to optimise acetogenesis in the bioreactor.
Syntrophic acetogenic bacteria include (a) the butyrate-
degrading acetogenic bacteria such as Syntrophomonas (d) Stage four: Methanogenesis
wolfei, Syntrophomonas sapovorans and Syntrophomonas
bryantii; (b) the propionate-degrading acetogenic bac- Methanogenesis is the biomethanisation step in which
teria such as Syntrophobacter wolinii, Syntrophobacter organic substrates: acetate, H2/CO2, methanol and for-
mate, the end products of the acetogenesis, are con-
verted into methane [65]. Unlike in the previous stages,
the microorganisms responsible for the methanogenic
stage belong to the domain archaea and they produce
methane via two major pathways: acetotrophic (or ace-
toclastic) and hydrogenotrophic methanogenic path-
ways (Table3). It has been estimated from stoichiometric
reactions that about 70% of the methane is produced via
the acetotrophic pathway [97]. Nevertheless, very few
known species can perform acetotrophic methanogen-
esis, whereas nearly all known methanogenic species are
hydrogenotrophic methanogens [27]. Bioenergetically,
hydrogenotrophic methanogenic reactions are more
favourable (G0 = 131.01 kJ/mol for H2/CO2 and
G0 = 135.6 kJ/mol for H2/HCO3), while acetoclastic
(acetotrophic) methanogenic reactions are least favour-
Fig.12 The energetics and effects of hydrogen partial pressure on able (G0=31.0kJ/mol for CH3COOH) as shown in
syntrophic degradation in anaerobic digestion Adapted from [27] Table 1. The hydrogenotrophic methanogenic pathway
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 16 of 29

is more energy yielding than acetotrophic methanogenic belonging to the genus Methanosarcina hence the former
pathway and is normally not rate limiting but rather fun- dominates the bioreactor at high acetate concentrations
damentally important in keeping the PH2 low in bioreac- and the latter at low acetate concentrations. Other meth-
tor system, allowing syntrophic acetogenesis to proceed. anogenic groups include methylotrophic methanogens,
Hydrogen is recognised as the controlling parameter in which utilise methane-containing compounds such as
the overall scheme of waste biodegradation but rarely methanol, methylamine and dimethylsulphides [52].
detected in well-functioning methanogenic biodigest-
ers [14, 27]. Unlike the acetoclastic methanogens, the Products fromanaerobic digestion In AD, organic waste
hydrogenotrophic methanogens are among the fastest- is fed to the process as feedstock and acted upon by
growing organisms in the anaerobic biodegradation pro- microorganisms in the absence of oxygen [9, 53, 79, 80]
cess and the accumulation of hydrogen may only occur to produce biogas and bioslurry. The digestate (bioslurry)
during process overloads or toxic microbial inhibition. can be dewatered and converted through thermal con-
The minimum doubling time for the hydrogenotrophic version technologies into other forms of fuel including
methanogens has been estimated to be 6h compared to refuse-derived fuel (Fig. 13). The remaining inorganic
62.4h (2.6days) for the slow-growing acetoclastic metha- and the inert waste are either incinerated or gasified to
nogens [27]. Furthermore, hydrogenotrophic methano- generate more energy. Apart from energy generation,
gens are more resistant to environmental changes while the bioslurry can safely be used as biofertiliser in agri-
acetoclastic methanogens are more sensitive which cultural production as well as animal feed especially for
makes their reactions more rate limiting in several cases piggery, fisheries and aquaculture. This makes anaerobic
of anaerobic digestion of organic wastes [27]. The gen- digestion as one of the best waste-to-energy technologies
era Methanosaeta and Methanosarcina are the only two with superior advantage of coupling energy generation
groups known to carry out the acetotrophic methano- with the generation of valuable bi-products such as plant
genesis [61]. The microorganisms of the genus Metha- organic fertiliser (bioslurry) at minimal net operational
nosaeta have a lower maximum growth rate than those energy requirement. Furthermore, a study by Tock etal.

Fig.13 Generalised scheme of major products from anaerobic digestion [163]


Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 17 of 29

[163] reported that AD is usually a preferred WtE tech- starch into oligosaccharides and simple sugars; protease
nology for biomass with high water content (including for degrading protein into amino acids, and lipase for
banana waste). It is a low-temperature process that can degrading lipid into glycerol and long-chain fatty acids
process wet or dry feeds (with added water) economically [130]. The overall hydrolysis rate depends on organic
at a variety of scales. Results from previous studies on AD material size, shape, surface area, enzyme production
of banana peels [44] suggest the high potential and suit- and adsorption [21]. Moreover, competitive adsorp-
ability of banana waste as a feedstock for economically tion of enzyme on the inert substrate like lignin can also
viable waste treatment technology like anaerobic diges- decrease hydrolysis efficiency [46]. Hydrolysis has been
tion for the purpose of energy generation in the form of shown to be a rate-limiting step for the digestion of high
methane [163]. The composition of the gas produced is particulate substrate like agro-industrial residues, munic-
primarily carbon dioxide and methane with small traces ipal solid wastes, swine waste, cattle manure and sewage
of hydrogen sulphide. sludge while methanogenesis is the rate-limiting step for
Besides, the AD of banana waste also reduces global readily degradable substrate, due to the inherent slow
warming and air pollution since the methane produced is growth nature of methanogens (see later) [28].
considered a clean gas with a zero carbon cycle. Notably, the Floatation of feed slurry in bioreactors digesting the
banana biogas has been proven as a perfectly feasible option plant biomass is another challenge limiting the use of
to run tractors, farm machinery and vehicles [26], thus off- lignocellulosic material as feedstocks for biogas pro-
setting the industrial energy needs. Other advantages of AD duction. The anaerobic digestion of biomass from plant
process are: reduction in wastes pathogens, smaller land origin in conventional reactors including the high-rate
suitability and decrease in wastes pollution potential to lev- reactors is generally nuisance and problematic due to
els that are non-toxic to the environment [113]. the physical nature of the biomass, since these fibre-
rich plant biomass materials tend to build up a per-
Challenges of using lignocellulosic biomass as feedstocks sistent float layer. The floatation of the feed substrate
for anaerobic digestion Anaerobic digestion of plant leads to wash out of active biomass (inocula seeding)
biomass as digester feedstocks can be limited by three that results in digester failure. When feed substrates
typical challenges, namely: limited microbial hydrolysis of are discharged early from the reactor, the active flora
lignocellulosic biomass, floatation of feed slurry, as well adsorbed on to the biocarrier gets lost as well, further
as unbalanced C:N ratio. Limited microbial hydrolysis is reducing the efficiency [63]. This has limited the appli-
one of the major hindrances to AD of lignocellulosic plant cation of high-rate digesters such as upflow anaerobic
biomass such as banana waste, whereby, as much as 50% sludge blanket (UASB) and expanded granular sludge
of the feed substrate could be left undigested. bed (EGSB) reactors, in the treatment of buoyant waste
Lignocellulosic substrates are complex polymeric sub- biomass from plant origin and lipid-rich wastes such
stances that are insoluble and too large to be taken up by as fish processing and slaughter house effluents [34,
microbial cells for the subsequent intracellular anaero- 77, 134]). In order to prevent flotation, intensified agi-
bic degradation steps. Moreover, lignin degradation is tation and stirring have been recommended and this
primarily an aerobic process, and in an anaerobic envi- can demand up to 10% of the electric energy produced
ronment lignin can persist for very long periods [176]. after the conversion of the produced biogas into elec-
Therefore to use these lignocellulosic biopolymers as tricity. Intensive mixing can also negatively affect the
substrates for anaerobic digestion, they must undergo substrate decomposition process by inhibiting micro-
prior solubilisation under aerobic environment. Since bial flocculation and adsorption apart from taking up
biogas digesters are anaerobic, lignocellulosic feedstocks a considerable amount of energy that makes the system
have to first be degraded through pre-treatment stages economically unattractive. Generally typical biogas
such as biological hydrolysis under aerobic conditions digesters in use today cannot efficiently digest ligno-
prior to anaerobic digestion. A research by Mshandete cellulosic biomass from plant origin such as energy
etal. [119] reported that lignocellulosic-rich wastes such crops without modifications [Leibniz Institute for Agri-
as solid sisal residues have high suitability as feedstock cultural Engineering Potsdam-Bornim (ATB)]. Other
for biogas production, after effective hydrolysis. The research studies reported that AD can proceed at high
microbial hydrolysis of lignocellulosic biomass involves rate when carried out in appropriately designed biore-
several steps, including enzyme production, diffusion, actor system with fully optimised environmental and
adsorption, reaction and enzyme deactivation step [20]. operational parameters [25, 121].
Hydrolytic enzymes include laccase, cellulase, xylanase In addition, unbalanced C:N ratio is the other typi-
and amylase for degrading lignin, cellulose, xylan and cal challenge faced during anaerobic digestion of
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 18 of 29

lignocellulosic feedstocks from plant biomass. Hydroly- feedstock particle size directly affects the performance
sis of lignocellulosic plant biomass mainly releases a lot of anaerobic bioreactor operating on solid wastes, espe-
of sugars comprising simple sugars and oligomers such cially those with a high fibre content [129, 144, 166, 187].
as multitrioses, with limited nitrogen-rich biomolecules The mechanical size reduction of the particles and the
such as amino acids. This implies that there is a high C:N resulting increase in the available surface area represent
ratio in lignocellulosic plant biomass which can lead to an option for increasing biodegradation yields and accel-
acidic and inhibitory growth conditions for methano- erating the AD of substrates that have high fibre content
genic bacteria in anaerobic digesters. Successful hydroly- such as banana waste, sisal fibres and straw [11, 68, 119].
sis of lignocellulosic feedstocks such as banana waste can A research study by Mshandete etal. [119] demonstrated
yield a lot of sugars which if converted into organic acids that feedstocks with high content of fibres such as hay,
by the acidogenic bacteria, results into bioreactor acidifi- seeds and leaves give improved digester gas production
cation and inhibition of methanogenesis step. Therefore, after mechanical pre-treatment. This leads to a decrease
before one uses lignocellulosic biomass such as banana in the amount of residues to be disposed of, and to an
waste as a feedstock for biogas production, such apparent increase in quantity of useful digester gas. Therefore it is
challenges ought to be overcome. imperative to pulverise fibrous feedstocks prior to other
pre-treatment methods and subsequently anaerobic
Options for enhancement of AD of lignocellulosic feed- digestion.
stock The AD process is influenced by a number of fac- On the other hand, biological pre-treatment methods
tors leading to varying rates of methane production from have been reported to be cost-effective and the methods
a feedstock. The total methane yield and the rate of pro- employed are usually simple and involve mild conditions
duction, which are a measure of the degree of feedstock [111]. Biological pre-treatment includes pre-compost-
microbial digestion, is affected by factors namely: physi- ing and feedstock pre-hydrolysis by either hydrolytic
calchemical composition of feedstock (feedstock par- enzymes or pre-culture with hydrolytic enzyme-produc-
ticulate nature), C:N ratio, operating temperature, reten- ing microorganisms [175]. These strategies involve the
tion time, inhibitors, agitation (rate of stirring), loading utilisation of specific microorganisms and/or microbial-
rate and bioreactor configuration. Hence, the AD of plant derived materials (enzymes) as a means of improving a
biomass feedstock such as banana waste can be enhanced specific step in the AD process that limits the process.
through the optimisation of: (a) feedstock pre-treatment, Based on operational approach, the biological strategies
(b) C:N ratio by co-digestion; (c) bioreactor design; and include addition of microorganisms or enzymes prior to
(d) environmental and operational parameters. AD process ([41, 173]; Jeganathan et al. 2007). Others
include addition of enzymes directly into the reactor in
(a) Feedstock pre-treatment either a free or an immobilised form [42, 87] and bioaug-
mentation where specific microorganisms are introduced
Pre-treatment is generally feedstock deformation to directly into the digester [43]. Microorganisms, which are
increase its ability for hydrolysis and absorption by liv- naturally growing in lignocellulose-rich waste and other
ing cells. For lignocellulosic feedstock, an ideal pre-treat- phytomass-rich dumping site, get adapted to degrade lig-
ment method would increase surface area and reduce nocellulose waste. A number of microorganisms with the
lignin content and crystallinity of cellulose [57]. Ligno- potential for lignocellulose hydrolysis have been previ-
cellulosic biopolymer pre-treatment can be divided into ously isolated from such environment and characterised.
three categories (Table 4) namely: (a) physical methods They include the white-rot fungi of the genera Phanero-
such as mechanical (milling and grinding), irradiation, chaete, Lentinus and Trametes Wu etal. [185] and pleu-
steam explosion and hydrothermolysis; (b) thermo- rotus [132], and bacterial cellulase producers from the
chemical methods (treatment with alkali, dilute acid, Bacillus subtilis [95]. Nevertheless, the only organisms
oxidising agents, organic solvents and wet oxidation); known to extensively degrade lignin are fungi [92]. Nota-
and (c) biological methods such as whole microbial pre- bly, white-rot fungi are the only known living microor-
treatment, enzymatic hydrolysis and bioaugmentation ganism capable of complete lignin degradation, and their
([119, 120]; Bjrnsson et al. 2005). Physical/mechanical application has been suggested for delignification of lig-
and chemical pre-treatment methods have been quite nocellulosic substrates such as wheat straw [122] prior
intensively studied with the aim of improving the hydrol- to AD. The initial reactions are mediated by extracellular
ysis of lignocellulosic substrates. However, these methods lignin and manganese peroxidases, primarily produced
have the disadvantages of being either energy intensive by white-rot fungi [92]. Actinomycetes can also decom-
or costly and resulting into residual disposal problems pose lignin, but typically degrade less than 20 % of the
[159]. Nevertheless, many researchers have reported that total lignin present [18, 47]. Because lignin is an insoluble
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 19 of 29

Table4 Some common pre-treatment methods forlignocellulosic biomass (Adapted from [7, 91, 106, 160, 191])
Pre-treatment method Advantages Disadvantages

Physical
Mechanical: Physical reduction in substrate Reduced cellulose crystallinity and degree of Usually negative energy balance
particle size by grinding, milling, etc. polymerization
Increased surface area
Irradiation: Biomass undergoes high-energy Results in one or more changes to biomass Slow
radiation (i.e. -ray, ultrasound, electron Increased surface area Energy intensive
beam, pulsed electrical field, UV, microwave
heating) Reduced cellulose crystallinity and polymeriza- Prohibitively expensive
tion
Partial depolymerization of lignin
Steam explosion: Substrate particles rapidly Causes hemicellulose solubilization and lignin Destruction of a portion of the xylan fraction
heated by high-pressure saturated stream. transformation
Explosive decompression caused by quick Cost-effective Generation of toxin compounds
release of pressure acids released aid in hemi-
cellulose hydrolysis
Hydrothermal: Substrate is subject to high- Hemicellulose solubilization High water and energy demand
temperature/high-pressure water Partial delignification
Chemical
Alkaline: Addition of base causes swelling, Lignin solubilization Relatively long residence times required
increasing internal surface of cellulose which Reduced cellulose crystallinity and degree of Irrecoverable salts formed and incorporated into
provokes lignin structure disruption (NaOH, polymerization biomass
KOH, Lime, Mg(OH)2, NH4OH)
Increased surface area
Can be done at ambient temperature
Relatively inexpensive
Acid: Addition of dilute or concentrated acid Hemicellulose hydrolysis and converted to Relatively expensive
solutions result in hemicellulose hydrolysis fermentable sugars
(H2SO4, HCl, HNO3, H3PO4) Alters lignin structure Corrosive
With high acid concentration can be done at High operational and maintenance costs
room temp. Some inhibitory compounds formed
Catalysed stream explosion: Similar to steam Hemicellulose solubilization Some inhibitory compounds formed
explosion with addition of acid catalyst (SO2, Portion of xylan fraction lost
H2SO4, CO2, oxalic acid)
Incomplete disruption of lignin-carbohydrate
matrix
Ammonia fibre explosion (AFEX): Substrate is Delignification Hemicellulose not significantly removed
exposed to hot liquid ammonia under high Increases surface area Very high-pressure requirements
pressure. Pressure is released suddenly break-
ing open biomass structure Reduced cellulose crystallinity Expensive
Low formation of inhibitors
Wet oxidation: Dissolved oxygen oxidises Efficient removal of lignin High cost of oxygen and alkaline catalyst
substrate Low formation of inhibitors High temps and pressures
Exothermic
Organo-solvent extraction: Organic solvents are Delignification Solvent removal is necessary
applied, with or without addition of an acid Some hemicellulose solubilization Relatively expensive
or alkali catalyst to degrade internal lignin
and hemicelluloses bonds Recovery of relatively pure lignin as by-product
Biological
Fungi and actinomycetes: Microorganisms Degrades lignin and hemicellulose Low rate of hydrolysis
degrade/alter biomass structure (white-, Low energy consumption
brown-, soft-rot fungi )

polymer, the initial steps in its biodegradation must be (b) Substrate co-digestion
extracellular. Many enzymes are involved in the oxidative
degradation of lignin, including lignin peroxidases (LiP), Co-digestion is the anaerobic treatment of a mixture of
manganese peroxidase (MnP) and laccase [158]. at least two different nutrient-complementary substrates
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 20 of 29

or waste types. Co-digestion can overcome carbon or digesters to improve anaerobic digestion by sustain-
nitrogen deficiencies [182]. The mixing of several waste ing inoculum-substrate exposure and sludge retention
types has a positive synergy on both the AD process itself are inappropriate for AD of plant biomass and only best
and on economy of the treatment [78]. Abundance of suitable for liquid wastes such as waste water effluents.
nitrogen in the substrate can lead to excessive ammonia These bioreactors include upflow anaerobic sludge blan-
formation leading to ammonia toxicity and AD process ket (UASB) and expanded granular sludge bed (EGSB)
inhibition. Conversely, too little nitrogen creates a risk reactors. When anaerobic digestion of plant biomass is
of nutrient limitation and low buffering capacity inca- carried out in these conventional bioreactors, the feed
pable to neutralise the volatile fatty acids produced by substrate slurry tends to build up a persistent float layer
fermentative bacteria, ultimately resulting in a more pH- that results into discharge of effluent slurry containing
sensitive and inhibited AD process [121]. During AD, partially digested feed substrate and wash out of active
the microbial community utilises carbon 2530 times biomass (inocula seeding) and ultimately causing AD
faster than nitrogen [187]. Since not all the carbon and process failure. Therefore, the efficient anaerobic diges-
nitrogen in the substrate are available for digestion, the tion of lignocellulosic biomass with enhanced biogas pro-
actual C:N ratio is a function of the substrate character- duction rates requires an appropriate digester design that
istics and digestion operational parameters. Substrates can circumvent the above heighted challenge.
high in nitrogen can be combined with substrates high in Biogas digester design must address three major con-
carbon in order to attain the desired C:N ratio for opti- siderations, namely: physical nature and solid content of
mal AD process. In general, a C/N ratio of 2032 has feedstock, operating configuration mode and bioreac-
been reported to be the optimal for anaerobic digestion tor accessory devices. These factors need to be consid-
[31, 38, 166, 189]. Furthermore, co-digestion enables the ered interdependently when designing a bioreactor. The
treatment of organic waste with high methane yield due physical nature of feedstocks for anaerobic digestion can
to positive synergies established in the bioreactor [70, be categorised as either solid feedstocks such as fibrous
124]. Therefore a suitable ratio of biodegradable carbon (lignocellulosic) plant biomass, animal tissues (from ren-
to nitrogen can be maintained by co-digestion for effi- dering plants) or liquid feedstock such as high strength
cient AD process. Highly lignocellulosic feedstocks such wastewaters and sludge. These physical characteristics
as wood dust, cotton residues, among others which are dictate the design of bioreactor to be used for anaero-
rich in carbon but poor in nitrogen should be co-digested bic digestion with less complications and optimal biogas
with those rich in nitrogen but poor in carbon such as production. Generally, feedstocks with less than 15%
chicken droppings, pig slurry among others. Despite the solid content are termed as wet-pumpable substrates and
benefits of co-digestion, co-digestion of mixtures of dif- are appropriately digested by wet bioreactors. On the
ferent wastes including banana waste is seldom reported other hand, feedstock with a solid content of over 25% is
[48]. termed as drystackable substrate and is appropriately
digested by dry bioreactors. Bioreactors can be designed,
(c) Appropriate bioreactor design engineered and configured to operate in either batch or
continuous process mode. In a batch system, biomass is
An anaerobic bioreactor or biogas digester is an added to the bioreactor at the start of the process and
enclosed chamber that uses microorganisms to degrade then sealed for the duration of the process. All the four
organic matter with the production of biogas. Most farm- anaerobic digestion stages occur in one chamber. Batch
based biogas digesters are generally designed for the fer- bioreactors are feasible for highly malodorous and infec-
mentation of liquid manure and include the traditional tious feedstocks such as hospital wastewaters. Constant
floating dome Indian digesters, fixed dome Chinese production of biogas is achieved using more than one
digester and tubular type. Although these digester types batch reactor in series and consequently requires a lot
are commonly used in domestic biogas generation, they of space. In continuous digestion process mode, organic
are associated with significant gas leaks, mainly methane matter is simultaneously added as the digested material
and such defects mainly arise from technical and inap- is being removed usually by an automated system. Exam-
propriate designs which ultimately compromise the effi- ples of this form of anaerobic digestion include con-
ciency and overall economic value of the digester [72]. tinuous stirred-tank reactors, upflow anaerobic sludge
This indicates that they are not appropriate for industrial blankets, expanded granular sludge beds and internal
application in the current form and may either be modi- circulation reactors. Such bioreactors are appropriate
fied or new designs may be made for large-scale indus- for liquid slurry such as wastewaters and have constant
trial applications. Similarly, the high-rate and hybrid biogas production. Thick slurry with high solid content
digesters that have been modified from conventional (between 15 and 25%) can be digested by wet bioreactors
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 21 of 29

with more energy input to pump the substrate during


feeding and slurry removal. The thickness of the mate-
rial may also lead to bioreactor abrasion and clogging of
pipes. On the other hand, dry bioreactors are designed to
digest solid substrates of solid content between 25 and
40% without the addition of water, in a process termed as
solid-state anaerobic digestion. The primary styles of dry
bioreactors are continuous vertical plug flow and batch
tunnel horizontal dry bioreactors. Continuous vertical Fig.14 Phase separation of anaerobic digestion system. Adapted
plug flow dry bioreactors are upright, cylindrical tanks from [15]
where feedstock is continuously fed into the top of the
digester, and flows downward by gravity during digestion.
In batch tunnel dry bioreactor, the feedstock is deposited and is referred to as the methane-phase reactor. In this
in tunnel-like chambers with a gas-tight door. Another case, pH and temperature conditions can be maintained
design consideration is the necessary accessory device to at appropriate levels in either reactor. Two-phase diges-
be fitted with the bioreactor for optimal operation. This tion can also increase process stability by optimising the
consideration is majorly linked with the physical nature hydraulic retention time (HRT) for either phase of the
of the feedstock to be digested. These devices include process. Typically, HRT is shorter in the acid phase and
feed macerator to reduce particle size and increase sur- longer in the methane phase to accommodate for the
face area for microbial attachment degradation; mixer to variation in growth rate between the rapidly regenerating
re-circulate the feed with microorganism as well as foam acidogens and slow-growing methanogens. This can help
reduction; foam controller to disintegrate foam header prevent organic overloading or toxic acid buildup in the
on the surface of bioreactor liquor; and grit remover to methane phase [51].
trap sand and other indigestible material from entering Ultimately, two-phase operation allows for the selec-
the bioreactor. tion and enrichment of different bacteria in each phase.
Besides, the anaerobic digestion (AD) of feedstock Previous research has shown that two-phase anaerobic
in single-phase bioreactors, where all the four stages digestion can be successful in treating lignocellulosic
of AD process occur in one unpartitioned chamber, is substrates such as forest residues [73] and wood hydro-
always prone to upsets due to contrasting optimal con- lysate [36]. A report by Zhang [190] also revealed that the
ditions required for both acid and methane formation. acetate-utilising methanogens was 210 times higher in
The hydrolytic and acid-forming bacteria differ from the the two-phase system than in the single-phase system.
methane-forming bacteria in terms of their nutritional Therefore a well-designed two-phase bioreactor system
needs, growth kinetics and sensitivity to environmental can circumvent the problems associated with bioreactor
(bioreactor liquor) conditions such as pH. In conven- acidification and enhance the AD process leading to high
tional single-phase bioreactor, the system operates in a methane yields.
narrow delicate balance between acid phase and methane
phase (Fig.14) that must be maintained within the reac- (d) Optimisation of environmental and operational
tor in order to in avoid system failure due to acidification. parameters
After successful pre-treatment, the hydrolysis stage of
lignocellulosic feedstocks such as banana waste can yield Environmental parameters are conditions that can
a lot of sugars that when converted to organic acids by be routinely modulated (optimised) either manually or
the acidogenic bacteria can result into bioreactor acidifi- automatically to create suitable environment for micro-
cation and failure. These problems can be circumvented organisms and consequently enhancing the anaerobic
by carrying out a two-phase anaerobic digestion. In the digestion process [42, 60]. These environmental condi-
two-phase anaerobic digestion, the process is physically tions include volatile fatty acids (VFAs), pH, temperature,
separated into two reactors which offer a method for opti- alkalinity, microbial granulation and their optimal levels
mising the operating conditions for the various groups (Table 5) are closely affected by the operational param-
of microorganisms involved in the digestion process. In eters. The operational parameters include Organic load-
the two-phase system the first reactor, referred to as the ing rates (OLR), agitation/stirring, hydraulic retention
acid-phase reactor is operated under optimal conditions time (HRT), biomass retention and effluent recirculation
for hydrolysis and acidogenesis while the second reactor among others. Disturbances in reactor equilibrium can
is operated under optimal conditions for methanogenesis result in process inhibition and possible reactor failure.
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 22 of 29

Table5 Optimal environmental parameters fora stable anaerobic digestion


Environment parameter Stage ofanaerobic digestion process Optimal range References

pH Hydrolysis and acidogenesis (two-phrase anaerobic digestion) 5.56.5 [91]


Methanogenesis (two-phase anaerobic digestion) 6.58.5 [15, 91]
Mixed reactor liquid (one-phase anaerobic digestion) 6.77.8 [27, 42]
(PH2) (Hydrogen Partial pressure) Mixed reactor liquid (one-phase anaerobic digestion) 104105 atm [27, 42]
Alkalinity Mixed reactor liquid (one-phase anaerobic digestion) 12002300mg [118]
CaCO3 per litre
C:N ratio Mixed reactor liquid (one-phase anaerobic digestion) 2030 [15, 38]
NH3-Nitrogen Mixed reactor liquid (one-phase anaerobic digestion) 50200mg per litre [118]
Free NH3 Mixed reactor liquid (one-phase anaerobic digestion) <150mg per litre [118]
H2S Mixed reactor liquid (one-phase anaerobic digestion) <200mg per litre [54]
Heavy metals Mixed reactor liquid (one-phase anaerobic digestion) <104M [27]

(i) Retention time (RT) In addition to substrate characteristics, short HRT


is also limited by microbial regeneration rates. Metha-
In anaerobic digestion, retention time is defined as the nogens are relatively slow growers and require at least
average time spent by the substrate inside the digester 1015 days of retention in order to regenerate. Due to
before it comes out after the action of microorganisms this slow regeneration time of methanogens, reactor
in the bioreactor. Retention time is one the key factors startup require longer HRTs in order to allow enough
that controls the extent to which volatile solids in the time for inoculum sludge to reach a steady-state popula-
substrate are converted to biogas. In typical continuous tion [38]. Limitation of slow microbial regeneration rates
stirred-tank anaerobic digestion systems the solids reten- can also be overcome by appropriate reactor design con-
tion time (SRT) is equal to the hydraulic retention time taining microbial attachment biocarriers and membrane
(HRT). HRT is directly related to reactor volume, by the filters that retain microbial biomass during effluent slurry
equation: discharge. However, this might result into sludge buildup
leading to bioreactor clogging. Thus typical retention
HRT = (V )/(Q),
time for biogas units is in the range of 2060 days [67].
where V is reactor volume and Q is influent flow rate Moreover, optimal HRT may vary from 3050 days in
Short HRT results into faster wash out of active bio- tropical countries and goes up to 100days in colder cli-
mass than they can reproduce, consequently causing mates [187].
prolonged lag phase of some steps such as fermentative
step [60]. However, shorter retention times are preferred (ii) Organic loading rate
for waste treatment in order to reduce system costs and
increase process efficiency. Shorter HRT is achieved at Organic loading rate (OLR) is defined as the amount
higher anaerobic digestion rate that is mainly influenced of volatile solids or chemical oxygen demand fed to the
by substrate characteristics. Substrates containing high system per unit volume per day [106]. There is a balance
amounts of lignocellulose require relatively long HRTs between OLR and HRT that must be determined in order
in the range of 6090 days in order to achieve nearly to optimise digestion efficiency and reactor volume. As a
complete digestion of lignocellulosic substrates [141]. consequence, conventional high-rate reactors digesting
AD carried out in conventional bioreactor requires suf- energy crops can only handle around 34 kg of organic
ficient volume to give long retention time enough for effi- dry matter per cubic meter of working volume and per
cient and effective biodegradation of organics. However, day [63]. Higher OLR can lead to an inhibition of the
too long HRT requires large volume of the digesters that AD process due to the buildup of volatile fatty acids. At
are limited by cost, treatment capacity, net energy yield higher OLRs, retention times must be long enough such
and operational skills. Conventional anaerobic diges- that the microorganisms have enough time to sufficiently
tion processes operate at an HRT in the optimal range degrade the material. A study by Kirtane etal. [93] estab-
of 1530 days [103]. For continuous waste-generating lished that bioreactors fed with lignocellulosic biomass
industrial processing, an HRT of 15days would be opti- such as, fruit residues, banana waste among others at
mally ideal although it may be practically impossible for higher OLR of over 3.5 results into decrease in methane
AD of lignocellulosic waste without pre-treatment. yield due to microbial inhibition by tannins, alkaloids,
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 23 of 29

flavonoids and terpenoids originating from degradation often adopted for upflow anaerobic sludge blanket (UASB)
of plant cell wall. Nevertheless, higher OLRs can allow reactors treating acidic waste such as high carbohydrate
for smaller reactor volumes thereby reducing the associ- wastes to achieve the re-use of the internally generated
ated capital cost for waste treatment through anaerobic alkalinity to maintain the pH around neutral in the sludge
digestion. bed [121]. This leads to reduction in the operational costs
of treatment due to savings in alkalinity addition. Fur-
(iii) Feedstock C:N ratio thermore, recirculation of effluent liquor or leachate back
to the top of the same bioreactor promotes the disper-
Carbon to nitrogen ratio (C/N) is defined as the rela- sion of inoculants, nutrients and acids. The performance
tive amounts of elemental carbon and nitrogen present of dry batch anaerobic digestion has been reported to be
in the substrate [106]. In general, a C/N ratio of 2030 enhanced by leachate recirculation [160]. The same study
is considered optimal for anaerobic digestion [38, 189]. also reported that the leach-bed bioreactor design uses
Substrates with high C/N ratios, such as paper and most recirculation of leachate between new and mature biore-
crop residues are usually deficient in nitrogen, which is actors to inoculate, moisturise and provide nutrients for
an essential nutrient for microbial cell growth. Thus, rapid startup of new bioreactors (fresh waste bed) dur-
anaerobic digestion of very high C/N ratios such sisal ing anaerobic digestion of solid organic waste. Ultimately,
waste, wood dust and banana fruit-stalks may be limited recirculation of leachate removes any buildup of solubi-
by nitrogen availability. In the case of substrates with low lised products, which might otherwise inhibit degradation.
C/N ratios, such as some animal manure, toxic ammonia The organic acids produced during startup are conveyed to
buildup may become a problem. To overcome deficien- the mature bed where they converted to methane [96].
cies in either carbon or nitrogen, co-digestion of low C/N
ratio substrates with high C/N ratio substrates has been (v) pH
proven as an effective solution [69].
The pH influences the activity of microorganisms and
(iv) Bioreactor liquor mixing enzymatic activity as they are both active within certain
narrow pH ranges [42, 55]. However, due to the forma-
Mixing of bioreactor contents is an important fac- tion of different intermediates, pH varies within each
tor in achieving optimal biodegradation of substrate phase of anaerobic digestion. At the same time, the dif-
and enhanced methane yield [60]. The mixing assures ferent microbial groups involved in each phase require
that all biodegradable matter (metabolites) comes into different pH conditions for optimum growth. This strati-
contact with the biocatalysts (bacteria or enzymes) and fication of pH along phases of anaerobic digestion affects
removes products (such as biogas) from the system. Mix- the growth of certain microorganisms differently. In gen-
ing also serves to prevent pronounced temperature gradi- eral, hydrolytic and acidogenic bacteria prefer slightly
ents within the digester and provides a uniform bacterial acidic conditions near pH 6. Optimal pH for acidogens
population density as well as preventing scum formation has been reported in the ranges of pH 5.56.5 [91] and
and decantation of organic matter. Gentle or slow mix- 5.86.2 [192]. In contrast, acidic conditions are toxic to
ing is necessary to maintain process stability within the methanogenic bacteria, which prefer neutral conditions
reactor [189] and hence improving anaerobic digester in the range of pH 6.58.2 [91]. The growth rate of meth-
performance [39, 178]. However, excessive mixing espe- anogens falls sharply below pH 6.5 [116]. The pH-related
cially stirring at high rate using mechanical devices can inhibition of microorganisms in anaerobic digestion pro-
disrupt the anaerobic microorganisms, and therefore con- cess is caused by reactor imbalances between compounds
sideration must be taken in terms of intensity and dura- such as ammonia and volatile fatty acids. As a result,
tion of mixing. Effective mixing of digester contents can acid accumulation is one of the biggest potentials for
be carried out in a number of ways such as stirring using anaerobic digester failure. Thus to ensure stable opera-
mechanical devices and flushing nozzles, recirculation of tion in batch bioreactors (one-stage anaerobic digestion
biogas and effluent slurry as well as using a wave of feed process), pH should be maintained between 6.7 and 7.4
influx [177, 187]. Mshandete et al. [118] reported that [27, 42]. In a properly balanced reactor, pH is buffered
regular shaking (either manually or automatically by shak- through the generation of bicarbonate by methanogens
ers) of batch bioreactors especially at laboratory scale can [189]. Providing excess alkalinity through blending of
enhance anaerobic digestion. Other related studies have high carbohydrate waste feedstock with alkaline com-
revealed that optimal mixing can achieved by bioreactor pounds or appropriate substrate co-digestion can buffer
stirring at 60rpm for 15min/h [184]. In addition to con- the AD process against inhibition due to excess acid
vention bioreactor liquor mixing, liquid recirculation is accumulation.
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 24 of 29

(vi) Temperature production rates. It is therefore important to maintain


temperature constant and uniform throughout the diges-
Microorganisms are divided into three groups depend- tion process.
ing on their optimal growth temperature: psychrophilic
(1015 C), mesophilic (3040 C) and thermophilic Future trend
(4565 C). Similarly, anaerobic digestion occurs over a This review has indicated that anaerobic digestion is the
large range of temperature (Fig. 15); from psychrophilic most appropriate eco-friendly WtE option for the val-
temperature at around 10 C to some extreme thermo- orisation of banana waste. However, application of this
philic temperatures over 70C [4, 146]. However, anaero- technology to realise high-energy yields in the form of
bic digesters are usually operated in the mesophilic range methane requires a lot of modification with the feedstock,
with the optimal at 35C, or in the moderate thermophilic bioreactor design and optimisation of operational param-
range with the optimal at 55 C [108, 175]. Temperature eters. Although a number of lignocellulosic pre-treatment
significantly influences anaerobic reactions both from the methods have been greatly studied, there are still chal-
kinetic and thermodynamic point of view. Hydrolytic and lenges that need further investigation and improvement.
methanogenic biodegradation rates increase with temper- Chemical pre-treatment generally leads to residual chem-
ature up to certain temperature optima. ical disposal problems and extra cost for neutralisation of
In general, higher organic loading rates can be applied chemical-treated feedstock prior to anaerobic digestion.
in the thermophilic range because of higher microbial Hence, further research is needed to focus on microbial
growth rate and activity [55]. However, the activity of pre-treatment especially focusing on development of a
other groups of bacteria such as propionate and acetate viable microbial consortium with efficient lignocellulo-
degradation has been shown to decrease when tempera- lytic activity, since lignocellulosic degradation require
ture is increased above 60C [175]. In addition, the pro- sequential interplay of different individual microbial
cess reactions occurring in the thermophilic range are strains. Furthermore, the problems associated with plant
also more sensitive to toxicity [10, 55]. At higher temper- biomass clogging of conventional high-rate bioreactors
atures, some imbalances can occur such as those result- and process failure due to feedstock floatation need for
ing from higher acidogenesis (over VFA production) more research into development of solid-state anaero-
than methanogenesis (low conversion of VFA at higher bic digesters that are more tailored for biomethanisation
temperature). Most conventional anaerobic digestion of high solid feedstocks such as plant biomass including
processes occur under mesophilic temperatures due to energy crops and banana waste. Since banana waste has
stability mesophilic conditions that requires less energy high moisture content, it could be digested without addi-
input compared to operation under thermophilic condi- tional water requirement. The design and engineering of a
tions, and results in a higher degree of digestion com- future solid-state digester tailored for anaerobic digestion
pared to operation under psychrophilic conditions [38, of plant biomass should ensure that it:
91]. Within each temperature range, fluctuations in tem-
perature by even a few degrees can affect microbial activ- Operates in a semi-continuous mode to allow sustain-
ity. A study by Chae etal. [35] reported that a fluctuation able gas production all throughout without interrup-
from 35 to 30C caused a significant reduction in biogas tion like that caused by batch reactors.
Has mixing devices to mingle incoming (fresh) solid
feedstock with the leachate inoculums.
Re-circulates effluent slurry or leachate back to the
digester to re-inoculate the incoming solid feedstock
and minimise water usage.

Lastly, further research into standardisation of optimal


operational parameters for anaerobic digestion of lig-
nocellulosic feedstocks will be imperative for full-scale
application of the technology for industrial and large-
scale energy generation.

Conclusion
Fig.15 Temperature ranges for anaerobic digestion; optima are In this review, the waste-to-energy technologies that
35C for mesophilic range and 55C for thermophilic range. Adapted are potentially applicable to Ugandas banana industri-
from [108]
alisation were highlighted. Generally, both thermal and
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 25 of 29

thermo-chemical conversion technologies can positively Ethical approval


Authors of paper publications reviewed in this article were acknowledged as
generate net energy if the processes do not require addi- text citation and references. Otherwise, ethical approvals are not applicable.
tional fuel input. Direct thermal and thermo-chemical
conversion technologies would be inappropriate Waste- Funding
This work is part of research under post-harvest loss reduction and value addi-
to-Energy options for wastes with high moisture content tion (RELOAD) in East Africa and was financially supported by RELOAD project,
such as banana waste due to low net energy yield despite Makerere University, Kampala. Uganda.
their superior potential for complete pathogen destruc-
Received: 27 August 2016 Accepted: 16 December 2016
tion. The net energy yield of biomass through thermal
conversions is directly related to the moisture content
of substrate. Banana waste can be on positive net energy
balance through direct thermo-chemical conversions
when the substrate had prior drying before thermal deg- References
radation. Therefore, thermo-conversion options seem 1. Abdullah N, Sulaiman F, Miskam MA, Taib RM. Characterization
of banana (Musa spp.) pseudo-stem and fruit-bunch-stem as a
less favoured due to the high moisture content of banana potential renewable energy resource. Int J Biol Vet Agric Food Eng.
waste. On the other hand, biochemical conversion tech- 2014;8(8):712.
nologies are more favoured by such moisture content in 2. Acrolab. Isobar heat pipe. 2013. http://www.acrolab.com/products/
isobars-heat-pipes.php.
addition to being more eco-friendly. Among these tech- 3. Agar D, Wihersaari M. Bio-coal, torrefied lignocellulosic resources. Key
nologies, anaerobic digestion stands out as the most properties for its use in co-firing with fossil coal-their status. Biomass
feasible waste-to-energy technology for Uganda banana Bio Energy. 2012;44:10711.
4. Ahring BK. Status on science and application of thermophilic anaerobic
industrialisation mainly due to limited technical knowl- digestion. Water Sci Technol. 1994;30:2419.
edge and economic capability to employ more sophis- 5. Ali N, Ubhrani P, Tagotra M, Ahire M. A step towards environmental
ticated energy conversions such as supercritical water waste management and sustainable biofuel (ethanol) production from
waste banana peelings. Am J Eng Res. 2014;03(05):1106.
gasification, pyrolysis and bioethanol production. More- 6. Alibas L. Energy consumption and colour characteristics of nettle
over, anaerobic digestion is a more appropriate waste- leaves during microwave, vacuum and convective drying. Biosyst Eng.
to-energy technology for banana waste since the latter 2007;96(4):495502.
7. Alvira P, Tomas Pejo E, Ballesteros M, Negro MJ. Pretreatment technolo-
is high organic and purely biodegradable with release of gies for an efficient bioethanol production process based on enzymatic
carbohydrates especially starch and lignocelluloses that hydrolysis: a review. Bioresour Technol. 2010;101(13):485161.
have high net potential for production of energy in the 8. Amani T, Nosrati M, Sreekrishnan TR. Anaerobic digestion from the
viewpoint of microbiological, chemical, and operational aspectsa
form of biogas. Besides, the effluent digestate waste from review. Environ Rev. 2010;18:25578.
anaerobic digestion is a cheap source of nutrient-rich 9. Ambulkar A, Shekdar A. Prospects of biomethanation technology in
plant biofertiliser which can be re-applied to plantation the Indian context: a pragmatic approach. Resour Conserv Recycl.
2004;40:11128.
to boost crop production. 10. Angelidaki I, Ahring BK. Anaerobic thermophilic digestion of manure
at different ammonia loads: effect of temperature. Water Res.
1994;28:72731.
Abbreviations 11. Angelidaki I, Ahring BK. Methods for increasing the biogas potential
BW: banana waste; WtE: waste-to-energy; TOPs: torrefied pellets; ASP: aerated from the recalcitrant organic matter contained in manure. Water Sci
static pile; AD: anaerobic digestion; EC: enzyme code; PH2: hydrogen partial Technol. 2000;41:18994.
pressure; HRT: hydraulic retention time; OLR: organic loading rate; VFA: volatile 12. Annepu RK. Sustainable solid waste management in India. New York:
fatty acids. Columbia University in the city of New York, Department of Earth and
Environmental Engineering; 2012.
Authors contributions 13. Arancon RAD, Lin CSK, Chan KM, Kwan TH, Luque R. Advances on waste
RG wrote the draft of the manuscript, JFH coordinated the manuscript, MO valorization: new horizons for a more sustainable society. Energy Sci
and OH contributed to manuscript revision and approved the final version. All Eng. 2013;1(2):5371.
authors read and approved the final manuscript. 14. Archer DB. The microbial basis of process control in methanogenic
fermentation of soluble waste. Enzym Microb Technol. 1983;5:1629.
Author details 15. Aslanzadeh S. Pretreatment of cellulosic waste and high-rate biogas
1 production, Ph.D. thesis submitted to School of Engineering, University
School ofBiosciences, Makerere University, P.O Box7062, Kampala, Uganda.
2 of Bors. SE-501 90 Bors (Sweden). Printed in Sweden by Ineko AB
School ofEngineering, Makerere University, P.O Box7062, Kampala, Uganda.
3 Bors 2014; ISBN 978-91-87525-11-7 (pdf ); 2014.
Universitt Kassel-FG Agrartechnik, Nordbahnhofstr.1a, 37213Witzenhausen,
Germany. 16. Balagurusamy N, Ramasamy K. Biogas technology: an Indian perspec-
tive. Curr Sci. 1999;77:4455.
Acknowledgements 17. Balagurusamy N. A preliminary study on molecular characterization of
This research was supported by the RELOAD project. the eubacteria in a thermophilic, poultry waste fed anaerobic digester.
Revista Mexicana de Ingeniera Qumica. 2007;6:23742.
Competing interests 18. Basaglia M, Concheri G, Cardinali S, Pasti-Grigsby MB, Nuti MP. Enhanced
The authors declare that they have no competing interests. degradation of ammonium-pretreated wheat straw by lignocellulolytic
Streptomyces spp. Can J Micorbiol. 1992;38(10):10225.
Availability of supporting data 19. Batidzirai B, Mignot APR, Schakel WB, Junginger HM, Faaij APC. Biomass
All the data analysed in this review study was obtained from online published torrefaction technology: techno-economic status and future prospects.
articles indicated in the reference section. Otherwise, not applicable. Energy. 2013;62:196214.
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 26 of 29

20. Batstone DJ, Keller J, etal. The IWA anaerobic digestion Model No 1 46. Converse AO, Optekar JD. A synergistic kinetics model for enzymatic
(ADM1). Water Sci Technol. 2002;45(10):6573. cellulose hydrolysis compared to degree-of-synergism experimental
21. Batstone DJ, Keller J, Newell RB, Newland M. Modelling anaerobic results. Biotechnol Bioeng. 1993;42:1458.
degradation of complex wastewater I: model development. Bioresour 47. Crawford DL. The role of actinomycetes in the decomposition of ligno-
Technol. 2000;75:6774. cellulose. FEMS Symp. 1986;34:71528.
22. Bayer AE, Lamed R. Ultrastructure of the cell surface cellulosome of 48. De Baere L. Anaerobic digestion of wastes: state of the art. Waste Sci
Clostridium thermocellum and its interaction with cellulose. J Bacteriol. Technol. 2000;41:28390.
1986;167(3):82836. 49. Delbes C, Moletta R, Godon J-J. Monitoring of activity dynamics of an
23. Bayer AE, Setter E, Lamed R. Organization and distribution of the cel- anaerobic digester bacterial community using 16S rRNA polymerase
lulosome in Clostridium thermocellum. J Bacteriol. 1985;163(2):5529. chain reactionsingle-strand conformation polymorphism analysis.
24. Ben H, Ragauskas AJ. Torrefaction of Loblolly pine. Green Chem. Environ Microbiol. 2000;2:50615.
2012;14:726. 50. Delivand MK, Barz M, Gheewala SH. Logistics cost analysis of rice straw
25. Bilibio C, Hensel O, Selbach J. Sustainable water management in the trop- for biomass power generation in Thailand. Energy. 2011;36(3):143541.
ics and subtropics (and case studies in Brazil), vol. 2. Jaguaro: Fundao 51. Demirer GN, Chen S. Two-phase anaerobic digestion of unscreened
Universidade Ederal Do Pampa; UNIKASSEL-Pgcult-UFMA; 2011. dairy manure. Process Biochem. 2005;40:35429.
26. Biopact news. Growcom trials commercial biogas production from 52. Deppenmeir U, Mller V, Gottschalk G. Pathways of energy conservation
banana wastehigh potential yields; 2008. http://news.mongabay. in methanogenic archea. Archaea Microbiol. 1996;165:14963.
com/bioenergy/2008/01/growcom-trials-commerical-biogas.html. 53. Elango D, Pulikesi M, Bakaralingam P, Ramamurthi V, Sivanesan S.
27. Bjrnsson L. Intensification of the biogas process by imposed process Production of biogas from municipal waste with domestic sewage. J
monitoring and biomass retention. Doctoral dissertation, Department Hazard Mater. 2007;141:3014.
of Biotechnology, Lund University; 2000. 54. Eldem N, Ozturk I, Soyer E, Calh B, Akgiray . Ammonia and pH inhibi-
28. Bjrnsson L, Murto M, Jantsch TG, Mattiasson B. Evaluation of new meth- tion in anaerobic treatment of wastewaters. Part I: Exp. J. Environ. Sci.
ods for the monitoring of alkalinity, dissolved hydrogen and the microbial Health. 2004;39:240520.
community in anaerobic digestion. Water Res. 2001;35(12):283340. 55. El-Mashad HM, Zeeman G, Van Loon WKP, Bot GPA, Lettinga G. Effect of
29. Bobleter O. Hydrothermal degradation and fractionation of saccharides temperature and temperature fluctuation on thermophilic anaerobic
and polysaccharides. In: Dumitriu S, editor. Polysaccharides, Structural digestion of cattle manure. Bioresour Technol. 2004;95:191201.
diversity and versatility. New York, Basel, Hong Kong: Dekker Inc.; 1998. 56. Ensinas AV, Modesto M, Nebra S, Serra L. Reduction of irreversibility
30. Bosmans A, Vanderreydt I, Geysen D, Helsen L. The crucial role of Waste- generation in sugar and ethanol production from sugar cane. Energy.
to-Energy technologies in enhanced landfill mining: a technology 2009;34:6808.
review. J Clean Prod. 2013;55:1023. 57. Fan LT, Lee YH, Beardmore DH. The influence of major structural fea-
31. Bouallagui H, Cheikh RB, Marouani L, Hamdi M. Mesophilic biogas pro- tures of cellulose on rate of enzymatic hydrolysis. Biotechnol. Bioeng.
duction from fruit and vegetable waste in a tubular digester. Bioresour 1981;23:41924.
Technol. 2003;86:8585. 58. Fagundes M. Factors affecting the reduction of carbon to nitrogen ratio
32. Bridgwater AV. Catalysis in thermal biomass conversion. Applied Cataly- in composting separated solids. Senior Project Presented to the Faculty
sis A: General; 1994, pp. 547. of the Dairy Science Department California Polytechnic State University,
33. Bryant MP. Microbial methane production-theoretical aspects. J Anim San Luis Obispo; 2012.
Sci. 1979;48:193201. 59. Food and Agricultural Organisation Statistics (FAOSTAT) 2012 data on
34. Cammarota MC, Teixeira GA, Freire DMG. Enzymatic pre-hydrolysis and bananas and plantains production.
anaerobic degradation of wastewaters with high fat contents. Biotech- 60. Frick M, Uppsten M. Alkaline pretreatment of water Hyacinth for improved
nol Lett. 2001;23:15915. anaerobic digestion. Unpublished Master of Science thesis. Lund: Depart-
35. Chae KJ, Jang A, Yim SK, Kim I. The effects of digestion temperature and ment of Biotechnology, Lund University; 1999.
temperature shock on the biogas yields from the mesophilic anaerobic 61. Garcia JL, Patel BKC, Ollivier B. Taxonomin phylogenetic and ecological
digestion of swine manure. Bioresour Technol. 2008;99(1):16. diversity of methanogenetic Archaea. Anaerobe. 2000;6:20526.
36. Chakrabarti SK. Biphasic biomethanation of wood-hydrolysate effluent. 62. Gasafi E, Reinecke MY, Kruse A, Schebek L. Economic analysis of sewage
Artif Cells Blood Substit Immobil Biotechnol. 1999;27(56):4617. sludge gasification in supercritical water for hydrogen production.
37. Chambers A. Renewable energy in non-technical language. Houston: Biomass Bio Energy. 2008;32:108596.
PennWell Books; 2003. 63. German Agency for Renewable Energy. 2005. http://global.mongabay.
38. Chandra R, Takeuchi H, Hasegawa T. Methane production from com/news/bioenergy/2007/07/new-biogas-reactor-for-energy-crops.
lignocellulosic agricultural crop wastes: a review in context to html.
second generation of biofuel production. Renew Sustain Energy Rev. 64. Graefe S, Dufour D, Giraldo A, Muoz LA, Mora P, Sols H, Garcs H,
2012;16(3):146276. Gonzalez A. Energy and carbon footprints of ethanol production using
39. Chen T, Chynoweth DP, Biljetina R. Anaerobic digestion of municipal banana and cooking banana discard: a case study from Costa Rica and
solid waste in a nonmixed solids concentrating digester. Appl Biochem Ecuador. Biomass Bioenergy. 2011;35(7):26409.
Biotechnol. 1990;24(25):533. 65. Gujer W, Zehnder AJB. Conversion processes in anaerobic digestion.
40. Chen WH, Kuo PC. Torrefaction and co-torrefaction characterization of Water Sci Technol. 1983;15:12767.
hemicellulose, cellulose and lignin as well as torrefaction of some basic 66. Gumisiriza R, Mshandete AM, Rubindamayugi MST, Kansiime F, Kivaisi
constituents in biomass. Energy. 2011;36:80311. AK. Enhancement of Anaerobic digestion of Nileperch fish processing
41. Chipasa KB, Medrzycka K. Behaviour of Lipids in Biological Wastewater waste water. Afr J Biotechnol. 2009;8(2):32833.
Treatment Processes. Journal of Industrial Microbiol Biotechnology. 67. Gunnarsson G, Mattsson C. Water hyacinth-trying to turn an environ-
2006;33:63545. mental problem into an agriculture resource, M.Sc. thesis, Uppsala:
42. Cirne DG. Evaluation of biological strategies to enhance hydrolysis dur- Swedish University of Agriculture Science; 1997.
ing anaerobic digestion of complex waste. Lund: Doctoral dissertation, 68. Hartman H, Angelidaki I, Ahring BK. Increase of anaerobic degradation
Department of Biotechnology, Lund University; 2006. of particulate organic matter in full-scale biogas plants by mechanical
43. Cirne DG, Lehtomki A, Bjrnsson L, Blackall LL. Hydrolysis and micro- maceration. Water Sci Technol. 2000;41:14553.
bial community analyses in two-stage anaerobic digestion of energy 69. Hartmann H, Ahring B. Anaerobic digestion of the organic fraction of
crops. J Appl Microbiol. 2007;103:51627. municipal solid waste: influence of co-digestion with manure. Water
44. Clarke WP, Radnidge P, Lai TE, Jensen PD, Hardin MT. Digestion of waste Res. 2005;39(8):154352.
bananas to generate energy in Australia. Waste Manag. 2008;28:52733. 70. Hartmann H, Angelidaki I, Arhing BK. Co-digestion of the organic
45. Clini C, Musu I, Gullino ML. Sustainable development and environmen- fraction of municipal waste with other waste types. In: Mata-Alvarez
tal management: experiences and case studies. Berlin: Springer; 2008. J, editor. Biomethanization of the Organic Fraction of Municipal Solid
p. 2289. Wastes. London: IWA Publishing; 2003.
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 27 of 29

71. Harwood RC. Bacillus subtilis and its relatives: molecular biology and 97. Lalman JA, Bagley DM. Anaerobic degradation and methanogenic
industrial workhorses. Trends Biotechnol. 1992;10:24756. inhibitory effects of oleic and stearic acids. Water Res. 2001;35:297583.
72. Hensel., 2014: Hermann Sewerin GmbH, FG Mess- und Regelungstech- 98. Lee H, Smith Z. Feasibility of biomass fuel briquettes from banana plant
nik & FG Agrartechnik; sponsored by: Deutsche Stiftung Umwelt. waste. Cincinnati: Engineers Without Borders Greater Cincinnati Profes-
73. Hooper R, Li J. Summary of the factors critical to the commer- sional; 2011.
cial application of bioenergy technologies. Biomass Bioenergy. 99. Lee LY. Household energy mix in Uganda. Energy Econ. 2013;39:25261.
1996;11(6):46974. 100. Lehninger AL, Nelson DL, Cox MM. Principles of biochemistry. 2nd ed.
74. Hossain ABMS, Ahmed SA, Alshammari AM, Adnan FMA, Annuar MSM, New York: Worth Publishers; 1993. p. 479502.
Mustafa H, Hammad N. Bioethanol fuel production from rotten banana 101. Lewicki PP. Design of hot air drying for better foods. Trends Food Sci
as an environmental waste management and sustainable energy. Afr J Technol. 2006;17:15363.
Microbiol Res. 2011;5(6):58698. 102. Li D-C, Lu M, Li Y-L, Lu J. Purification and characterization of an endocel-
75. Hreggvidsson OG, Kaiste E, Holst O, Eggertsson G, Palsdottir A, lulase from the thermophilic fungus Chaetomium thermophilum CT2.
Kristjansson KJ. An extremely thermostable cellulose from the ther- Enzy Microbiol Technol. 2003;33:9327.
mophilic eubacteria Rhodothermus marinus. Appl Environ Microbiol. 103. Liebrand CB, Ling KC. Cooperative approaches for implementation of
1996;62(8):30479. dairy manure digesters. USDA Rural Development Research Report 217.
76. Hsieh W, Chen R, Wu T, Lin T. Engine performance and pollutant STOP 3252, 1400 Independence Ave., S.W Washington, DC 20250-3252;
emission of an SI engine using ethanol-gasoline blended fuels. Atmos 2009.
Environ. 2002;36:40310. 104. Luo X. Torrefaction of biomass; a comparative and kinetic study of
77. Hwu CS. Enhancing anaerobic treatment of wastewaters containing thermal decomposition for Norway spruce stump, poplar and fuel tree
oleic acid. Ph.D. Thesis. Wageningen Agricultural University; 1997. chips. M.Sc. thesis. Uppsala: Swedish University of Agricultural Sciences;
78. Hwu CS, Molenaar G, Garthoff J, van Lier JB, Lettinga G. Thermophilic 2011.
high-rate anaerobic treatment of wastewaters containing long 105. Mala BR, Aparn MT, Mohini SG, Vasanti VD. Molecular and biotech-
chain fatty acids; impact of reactor hydrodynamics. Biotechnol Lett. nological aspects of microbial poteases. Microbiol Mol Biol Rev.
1997;19:44751. 1998;62:597635.
79. Iglesias J, Castrilloa L, Pelaez N, Marana E, Maison O, Andres H. 106. Martin-Ryals. Evaluating the potential for improving anaerobic diges-
Biomethanization of municipal solid waste in a pilot plant. Water Res. tion of cellulosic waste via routine bioaugmentation and alkaline
2000;34:44754. pretreatment. A thesis Submitted in partial fulfillment of the require-
80. Igoni A, Ayotamuno M, Eze C, Ogaji S, Probert S. Designs of anaero- ments for the degree of Master of Science in Agricultural and Biological
bic digesters for producing biogas from municipal solid-waste. Appl Engineering in the Graduate College of the University of Illinois at
Energy. 2008;85:4308. Urbana-Champaign; 2012.
81. Insam H, Franke-Whittle I, Goberna M. Microbes in aerobic and anaero- 107. Masjuki H, Kalam A. An overview of biofuel as a renewable energy
bic waste treatment. In: Insam H, Franke-Whittle I, Goberna M, editors. source: development and challenges. Procedia Eng. 2013;56:3953.
Microbes at work. Berlin: Springer; 2010. p. 134. 108. Matta-Alvarez J. Anaerobic digestion of organic fraction of municipal
82. IRENA. Prospects for the African power sector scenarios and strategies for solid waste: a perspective. In: Matta-Alvarez J, editor. Biomethanization
Africa project. Int Renew Energy Agency; 2012. of the organic fraction of municipal solid waste. London: IWA Publish-
83. IRIN News, 2008. http://www.irinnews.org/feature/2008/01/23/study- ing; 2003. p. 91105.
says-quality-nile-water-has-improved. Accessed Aug 2016. 109. Mclnerney MJ. Anaerobic hydrolysis and fermentation of fats and
84. Irvine G, Lamont ER, Antizar-Ladislao B. Energy from waste: reuse proteins. In: Zehnder AJB, editor. Biology of anaerobic microorganisms.
of compost heat as a source of renewable energy. Int J Chem Eng. New York: Wiley; 1988. p. 373415.
2010;2010:110. 110. Medic D, Darr M, Shah A, Potter B, Zimmerman J. Effects of torrefac-
85. Islam MN. Kinetic analysis of air drying of potato: traditional and tion process parameters on biomass feedstock upgrading. Fuel.
improved methods. J Agric Eng Inst Eng Bangladesh. 1984;12:311. 2012;91:14754.
86. Islam MS, Haque MA, Islam MN. Effects of drying parameters on 111. Mendes AA, Castro HF, Pereira EB, Furigo A Jr. Application of lipases
dehydration of green banana (Musa sepientum) and its use in potato for wastewater treatment containing high levels of lipids. Quim Nova.
(Solanum tuberosum) chips formulation. Agric. 2012;10(1):8797. 2005;28:296305.
87. Jeganaesan J, George N, Amarjeet B. Oil wastewater treatment using a 112. Mohiuddin AKM, Saha MK, Hossain S, Ferdoushi A. Usefulness of
novel hybrid PBR-UASB system. Chemosphere. 2007;67:1492501. banana (Musa paradisiaca) wastes in manufacturing of bio-products: a
88. Kadam KL. Environmental benefits on a life cycle basis of using review. Agric. 2014;12(1):14858.
bagasse- derived ethanol as a gasoline oxygenate in India. Energy 113. Moody LB, Roman DR. A dual-anaerobic system for complete treatment
Policy. 2002;30:37184. of food processing waste. J Agric Eng Res. 2001;80:2939.
89. Kagezi GH, Kangire A, Tushemereirwe W, Bagamba F, Kikulwe E, 114. Morgenroth E, Kommedal R, Harremos P. Processes and modeling
Muhangi J, Gold CS, Ragama PC. Banana bacterial Wilt incindece in of hydrolysis of particulate organic matter in anaerobic wastewater
Uganda. Afr Crop Sci J. 2006;14(2):8391. treatmenta review. Water Sci Technol. 2002;15:2540.
90. Kalyani KA, Pandey KK. Waste to energy status in India: a short review. 115. Morgenroth E, Kommedal R, Harremoe P. Processes and modeling
Renew Sustain Energy Rev. 2014;31:11320. of hydrolysis of particulate organic matter in aerobic wastewater
91. Khalid A, Arshad M, Anjum M, Mahmood T, Dawson L. The anaerobic treatmenta review. Water Sci Technol. 2002;45(6):2540.
digestion of solid organic waste. Waste Manag. 2011;31(8):173744. 116. Mosey FE, Fernandes XA. Patterns of hydrogen in biogas from anaero-
92. Kirk TK, Farrell RL. Enzymatic combustion: the microbial degradation of bic digestion of milk-sugars. Water Sci Technol. 1989;21:18796.
lignin. Ann Rev Microbiol. 1987;41:465505. 117. Motevali A, Minaei S, Khoshtagaza MH. Evaluation of energy
93. Kirtane RD, Suryawanshi PC, Patil MR, Chaudhari AB, Kothari RM. consumption in different drying methods. Energy Convers Manag.
Optimization of organic loading rate for different fruit waste during 2011;52(2):11929.
biomethanization. J Sci Ind Res. 2009;68:2525. 118. Mshandete A, Kivaisi A, Rubindamayugi M, Mattiasson B. Anaerobic
94. Koyuncu T, Tosun I, Pnar Y. Drying characteristics and heat energy batch co-digestion of sisal pulp and fish wastes. Bioresour Technol.
requirement of cornelian cherry fruits (Cornus mas L.). J Food Eng. 2004;95:1924.
2007;78(2):7359. 119. Mshandete A, Bjrnsson L, Kivaisi AK, Rubindamayugi ST, Mattiasson
95. Krishna C. Production of bacterial cellulases by solid state bioprocess- B. Enhancement of anaerobic batch digestion of sisal pulp waste by
ing of banana wastes. Bioresour Technol. 1999;69:2319. mesophilic aerobic pre-treatment. Water Res. 2005;39:156975.
96. Lai TE, Nopharatana A, Pullammanappallil PC, Clarke WP. Cellulolytic 120. Mshandete A, Bjrnsson L, Kivaisi AK, Rubindamayugi MST, Mattiasson
activity in leachate during leach-bed anaerobic digestion of municipal B. Effect of particles size on biogas yield from sisal fibres waste. Renew
solid waste. Bioresour Technol. 2001;80(3):20510. Energy. 2006;31:238592.
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 28 of 29

121. Mshandete AM. Improved anaerobic digestion of agro-industrial waste 147. Schink B. Energetics of syntrophic cooperation in methanogenic degra-
by enhanced hydrolysis and operational design. Doctoral thesis. Dar es dation. Microbiol. Mol. Biol. Rev. 1997;61:26280.
salaam: University of Dar es salaam; 2005. 148. Schorr C, Muinonen M, Nurminen F. Torrefaction of biomass. Mikkeli:
122. Mller HW, Trsch W. Screening of white-rot fungi for biological Miktech Ltd/Centre of Expertise-programme; 2012. p. 55.
pretreatment of wheat straw for biogas production. Appl Microbiol 149. Sellin N, De Oliveira BG, Maranon C, Souza O, De Oliveira APN, Novais
Biotechnol. 1986;24:1805. De Oliveira TM. Use of banana culture waste to produce briquettes.
123. Mnster M, Meibom P. Optimization of use of waste in the future Chem Eng Trans. 2013;32:49354.
energy system. Energy. 2011;36(3):161222. 150. Shapouri H, Duffield JA, Wang M. The energy balance of corn ethanol:
124. Murto M, Bjornsson L, Mattiasson B. Impact of food industrial waste on an update. Washington, DC: United States Department of Agriculture,
anaerobic co- digestion of sewage sludge and pig manure. J Environ USDA; 2002.
Manage. 2004;70:1017. 151. Shaw CM, Stentiford EI. Heat transfer in composting systems. In: Ber-
125. Nagase M, Matsuo T. Interactions between amino acid-degrading bac- toldi Md, Sequi P, Lemmes B, Papi T, editors. Proceedings of the Science
teria and methaanogenic bacteria in anaerobic digestion. Biotechnol of Composting, vol. 2. Glasgow: Blackie Academic &Professional; 1996.
Bioeng. 1982;24:222739. pp. 1331334.
126. Nandkumar N. Plasmathe fourth state of matter. Int J Sci Technol 152. Singh RP, Tyagi VV, Allen T, Ibrahim MH, Kothari R. An overview for
Res. 2014;3(9):4952. exploring the possibilities of energy generation from municipal
127. Nordin A. The dawn of torrefaction BE-sustainable: the magazine of bio- solid waste (MSW) in Indian scenario. Renew Sustain Energy Rev.
energy and the bioeconomy. 2012. pp. 213. http://www.besustaina- 2011;15(9):4797808.
blemagazine.com/cms2/the-dawn-of-commercial-torrefaction/ 153. Sivakumaran S, Balagurusamy N, Ramasamy K. Cellulase complex in
128. Ortega-Charleston L. Hyperthermophilic anaerobic digestion of food biogas slurry. In: Kannaiyan S, Ramasamy K, Ilamuguru K, Kumar K, edi-
waste. Ph.D. thesis. Montreal: McGill University; 2008. tors. Biological nitrogen fixation and biogas technology. Coimbatore:
129. Palmowski L, Mller J. Influence of size reduction of organic waste on Tamil Nadu Agricultural University; 1991. p. 10110.
their anaerobic digestion. Water Sci Technol. 2000;41:15562. 154. Smith M, Aber J. Heat recovery from compost: a step-by-step guide on
130. Parawira W, Murto M, Read JS, Mattiasson B. Profile of hydrolases and building an aerated static pile heat recovery compost facility. Biocycle.
biogas production during two-stage mesophilic anaerobic digestion of 2014;55(2):27.
solid potato waste. Process Biochem. 2005;40:294552. 155. Spilsbury JS, Jagwe JN, Ferris RSB. Evaluating the marketing oppor-
131. Park S, Jang C. Effects of pyrolysis temperature on changes in fuel tunities for banana and its products in the principle banana growing
characteristics of biomass char. Energy. 2012;39:1871895. countries of ASARECA (Uganda). International Institute of Tropical
132. Patrick F, Mtui G, Mshandete AM, Amelia Kivaisi A. Optimization of lac- Agriculture. Foodnet; 2002. p. 60.
case and manganese peroxidase production in submerged culture of 156. Stehlk P. Contribution to advances in waste-to-energy technologies. J
Pleurotus sajor-caju. Afr J Biotechnol. 2011;10(50):1016677. Clean Prod. 2009;17:91931.
133. Pavlostathis SG, Giraldo-Gomez E. Kinetics of anaerobic treatment. 157. Stephenson K, Bron S, Harwood RC. Cellular lysis in Bacillus subtilis; the
Water Sci Technol. 1991;24:3559. effect of multiple extracellular protease deficiencies. Lett Appl Micro-
134. Pereira MA. Anaerobic biodegradation of long chain fatty acids: biol. 1999;29:1415.
biomethanisation of biomass-associated LCFA as a challenge for the 158. Sugiura M, Hirai H, Nishida T. Purification and characterization of a novel
anaerobic treatment of effluents with high lipid/LCFA content, Ph.D. lignin peroxidase from white-rot fungus Phanerochaete sordida YK-624.
thesis. Braga: Minho University; 2003. FEMS Microbiol Lett. 2003;224:28590.
135. Phanphanich M, Mani S. Impact of torrefaction on the grindabil- 159. Takashima M, Kudoh MJ, Bildan MC. Effect of thermochemical pre-
ity and fuel characteristics of forest biomass. Bioresour Technol. treatment on the anaerobic digestion of waste activated sludge.
2011;102(2):124653. Waste Sci Technol. 1996;35:20915.
136. Pimchuai A, Dutta A, Basu P. Torrefaction of agriculture residue to 160. ten Brummeler E. Full scale experience with the BIOCEL process. Water
enhance combustible properties. Energy Fuels. 2010;24(9):463845. Sci Technol. 2000;41:299304.
137. Preethi P, Balakrishna MG. Physical and chemical properties of banana 161. Themelis NJ. Control of heat generation during composting. BioCycle.
fibre extracted from commercial banana cultivars grown in Tamilnadu 2005;46(1):2830.
State. Agrotechnol. 2013;S11:008. doi:10.4172/2168-9881.S11-008. 162. Tillmans A, Schweizerries P. Energy for sustainable development knowl-
138. Priest FG. Extracellular enzyme synthesis in the genus Bacillus. Bacteriol edge communication regarding solar home systems in Uganda: the
Rev. 1977;41:71153. consumers perspective. Energy Sustain Dev. 2011;15(3):33746.
139. Prins MJ, Ptasinski KJ, Janssen FJJG. More efficient biomass gasification 163. Tock JY, Lai CL, Lee KT, Tan KT, Bhatia S. Banana biomass as potential
via torrefaction. Energy. 2006;31(15):345870. renewable energy resource: a Malaysian case study. Renew Sustain
140. Rentizelas A, Tolis A, Tatsiopoulos IP. Logistics issues of biomass: the Energy Rev. 2010;14(2):798805.
storage problem and the multi-biomass supply chain. Renew Sustain 164. Tripathi L, Tripathi JN, Tushemereirwe WK. Rapid and efficient
Energy Rev. 2009;13(4):88794. production of transgenic East African Highland Banana (Musa
141. Rivard C, Bordeaux F, Henson J, Smith P. Effects of addition of soluble spp.) using intercalary meristematic tissues. Afr J Biotechnol.
oxidants on the thermophilic anaerobic-digestion of biomass to meth- 2008;7(10):143845.
ane. Appl Biochem Biotechnol. 1988;17(13):24562. 165. Tucker MF. Extracting thermal energy from composting. BioCycle.
142. Roberts JS, Kidd DR, Padilla-Zakour O. Drying kinetics of grape seeds. J 2006;47(8):38.
Food Eng. 2008;89:4605. 166. Tumutegyereize P, Muranga FI, Kawongolo J, Nabugoomu F. Opti-
143. Samadi SH, Ghobadian B, Najafi G, Motevali A. Potential saving in mization of biogas production from banana peels. Afr J Biotechnol.
energy using combined heat and power technology for drying agricul- 2011;10(79):1824351.
tural products (banana slices). J Saudi Soc Agric Sci. 2014;13:17482. 167. Tushemereirwe WK, Kangire A, Smith J, Nakyanzi M, Karyeija R, Kataama
144. Sanders WTM, Veeken AHM, Zeeman G, van Lier JB. Analysis and opti- D, Musiitwa C. An outbreak of banana bacterial wilt in Mukono and
misation of the anaerobic digestion of the organic fraction of municipal Kayunga district. A new and devastating disease NARO/KARI. Afr. Crop
solid waste. In: Mata-Alvarez J, editor. Biomethanization of the organic Sci. J. 2001;14(2):8391.
fraction of municipal solid waste. London: IWA Publishing; 2003. p. 6388. 168. Twaha S, Ramli MAM, Murphy PM, Mukhtiar MU, Nsamba HK. Renew-
145. Scarlat N, Motola V, Dallemand JF, Monforti-Ferrario F, Mofor Linus. able based distributed generation in Uganda: resource potential and
Evaluation of energy potential of municipal solid waste from African status of exploitation. Renew Sustain Energy Rev. 2016;57:78698.
Urban areas. Renew Sustain Energy Rev. 2015;50:126986. 169. UBA. Draft of a German report with basic information for a BREF-Docu-
146. Scherer PA, Vollmer GR, Fakhouri T, Martensen S. Development of a ment: Waste Incineration; 2001.
methanogenic process to degrade exhaustively the organic fractions 170. Uddin MB, Islam MN. Development of shelf stable pineapple products
of municipal grey waste under thermophilic and hyperthermophilic by different methods of drying. J Agric Eng Inst Eng Bangladesh.
conditions. Water Sci Technol. 2000;41:1739. 1985;13(1):513.
Gumisiriza et al. Biotechnol Biofuels (2017) 10:11 Page 29 of 29

171. UNEP. Municipal solid waste: is it garbage or gold? UNEP Global Envi- 183. Wilaipon P. The effects of briquetting pressure on banana-peel
ronmental Alert Series; 2013. http://www.unep.org/pdf/UNEP_GEAS- briquette and the banana waste in Northern Thailand. Am J Appl Sci.
oct_2013.pdf. 2009;6(1):16771.
172. UN-HABITAT. Collection of municipal solid waste in developing 184. Willkie AC, Smith PH, Bordeaux FM. An economical bioreactor for
countries. Nairobi: United Nations Human Settlements Programme evaluating biogas potential of particulate biomass. Bioresour Technol.
(UN-HABI-TAT); 2010. 2004;92:1039.
173. Valladao ABG, Freire DMG, Cammarota MC. Enzymatic pre-hydrolysisap- 185. Wu J, Xiao YZ, Yu HQ. Degradation of lignin in pulp mill wastewaters by
plied to the anaerobic treatment of effluents from poultry slaughter- white-rot fungi on biofilm, Biores. Technol. 2005;96:135763.
houses. Int Biodeterior Biodegrad. 2007;60:21925. 186. Xing J, Criddle C, Hickey R. Effects of long-term periodic perturbation
174. Van Passel S, Dubois M, Eyckmans J, de Gheldere S, Ang F, Jones PT, on anaerobic community. Water Res. 1997;31:2195204.
Van Acker K. The economics of enhanced landfill mining: private and 187. Yadvika Santosh, Sreekrishnan TR, Kohli S, Rana V. Enhancement of
societal performance drivers. J Clean Prod. 2013;55:92102. biogas production from solid substrates using different techniquesa
175. van Lier JB, Tilche A, Ahring BK, Macario H, Moletta R, Dohanyos M, review. Bioresour Technol. 2004;95:110.
Hulshoff Pol LW, Lens P, Verstraete W. New perspectives in anaerobic 188. Yan W, Hastings JT, Acharjee TC, Coronella CJ, Vsquez VR. Mass and
digestion. Water Sci Technol. 2001;43:118. energy balances of wet torrefaction of lignocellulosic biomass. Energy
176. Van Soest PJ. Nutritional Ecology of the Ruminant. 2nd ed. Ithaca: Fuels. 2010;24(9):473842.
Cornell University Press; 1994. 189. Zaher U, Grau P, Benedetti L, Ayesa E, Vanrolleghem PA. Transformers
177. Van DM, Faber J. Anaerobic fermentation of solid organic waste in a for interfacing anaerobic digestion models to pre- and post-treatment
reactor. WO Patent 9607726; 1996. processes in a plant-wide modelling context. Environ Model Softw.
178. Vavilin VA. Anaerobic degradation of solid material: importance of initia- 2007;22:4058.
tion centers for methanogenesis, mixing intensity, and 2D distributed 190. Zhang TC. Comparison of one-phase and two-phase anaerobic diges-
model. Biotechnol Bioeng. 2004;89(1):11322. tion processes in characteristics of substrate degradation and bacterial
179. Velasquez-Arredondo HI, Ruiz-Colorado AA, De Oliveira Junior S. population levels. Water Sci Technol. 1991;23(79):115766.
Ethanol production process from banana fruit and its lignocellulosic 191. Zheng M, Li X, Li L, Yang X, He Y. Enhancing anaerobic biogasification
residues: energy analysis. Energy. 2010;35(7):30817. of corn stover through wet state NaOH pretreatent. Bioresour Technol.
180. Wanapat M, Cherdthong A. Use of real-time PCR technique in studying 2009;100:51405.
rumen cellulolytic bacteria population as affected by level of roughage 192. Zoetemeyer RV, Andenheuvel JJC, Cohen A. pH influence on acido-
in buffalo. Curr Microbiol. 2009;58:2949. genic dissimilation of glucose in an anaerobic digester. Water Res.
181. Wannapeera J, Worasuwannarak N. Upgrading of woody biomass by 1982;16(3):30311.
torrefaction under pressure. J Anal Appl Pyrol. 2012;96:1731780.
182. Wei YH, Brune D. Anaerobic co-digestion of algal sludge and waste
paper to produce methane. Bioresour. Technol. 2007;98:1304.

Submit your next manuscript to BioMed Central


and we will help you at every step:
We accept pre-submission inquiries
Our selector tool helps you to find the most relevant journal
We provide round the clock customer support
Convenient online submission
Thorough peer review
Inclusion in PubMed and all major indexing services
Maximum visibility for your research

Submit your manuscript at


www.biomedcentral.com/submit

Вам также может понравиться